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Dinoflagellate cysts and hydrographical change in Gullmar Fjord, west coast of Sweden
Science of the Total Environment 355 (2006) 204 – 231 www.elsevier.com/locate/scitotenv
Dinof lagellate cysts and hydrographical change in Gullmar Fjord, west coast of Sweden Rex Harlanda,T, Kjell Nordbergb, Helena L. Filipssonc b
a DinoData Services, 50 Long Acre, Bingham, Nottingham NG13 8AH, UK Department of Oceanography, Earth Sciences Centre, Go¨teborg University, P.O. Box 460, S-40530, Go¨teborg, Sweden c University of Bremen, FB 5 Geosciences, P.O. Box 330 440, DE-28334 Bremen, Germany
Received 20 September 2004; accepted 18 February 2005 Available online 9 June 2005
Abstract This high-resolution study of the latest Holocene dinoflagellate cyst record from Gullmar Fjord, on the west coast of Sweden, provides evidence for the recognition of two major dinoflagellate communities within the fjord over the last 85 years. These communities may have their origins with the history of cultural eutrophication within the region, but are more likely to be associated with the wider phenomenon of the North Atlantic Oscillation and/or the complex hydrographical response of the fjord to various changing climatic environments between 1915 and 1999. The changing dinoflagellate cyst populations are compared in detail with the many hydrographical parameters available from this well studied fjord with its long instrumental records. Indeed the dinoflagellate cysts fail to demonstrate a convincing ongoing eutrophication record for the fjord but do show a major change in the cyst assemblages at about 1969/1970 at a time when the NAO was changing from a negative phase to the present-day positive phase. Gullmar Fjord is important in the history of dinoflagellate cyst studies, being the site of the 1954 study by Erdtman in which viable cysts, produced within the phytoplankton, were first documented within the water column. D 2005 Elsevier B.V. All rights reserved. Keywords: Dinoflagellate cysts; Eutrophication; North Atlantic oscillation; Coastal upwelling; Gullmar Fjord; West coast of Sweden
1. Introduction Marine offshore cultural eutrophication in Scandinavian waters is considered to be a major pollution problem, and has been the focus of research among a large number of marine scientists, for about twenty
T Corresponding author. Tel.: +44 1949 875287. E-mail address: [email protected] (R. Harland). 0048-9697/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2005.02.030
years (e.g. Baden et al., 1990; Diaz and Rosenberg, 1995; Nixon, 1995 and references therein). The consensus is that there has been an increase in the amount of sewage and agricultural fertilisers in the North Sea, including the Skagerrak, Kattegat and Baltic Sea, since the 1960s (Aure et al., 1996; Rosenberg et al., 1996). This has led in some locations, especially those additionally subjected to local drainage outlets and sewage outfalls, to enhanced primary production, altered algal composi-
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tion, decreased secci depth, increased accumulation of oxygen consuming organic material on the sea floor, oxygen deficiency in bottom water and subsequent benthic mortality.
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Gullmar Fjord is one of a series of sill fjords along the west coast of Sweden, north of Go¨teborg, in which this problem has been manifest. The fjord (Fig. 1) is some 30 km long and 2 km wide and
Fig. 1. Location map of Gullmar Fjord showing the site of core G113, the source of local pollution from Lysekil and Munkedal and the locations of the stations from which the instrumental data have been sourced. Vinga Island is located approximately 10 km west of Gfteborg (Gbg).
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has a maximum depth of 119 m. It is orientated in a NE/SW direction and opens into the Skagerrak across a sill at 42 m depth. The fjord is subjected to strong stratification with pycnoclines occurring at depths of between 15 and 20 m (Svansson, 1984), separating upper low salinity waters (24–27 psu) from more saline waters (32–33 psu), and between 50 and 60 m separating those waters from the highly saline waters (34–35 psu) in the deeper parts of the fjord (Lindahl et al., 1998; Arneborg, 2004). This stratification arises from the presence of low salinity Baltic water at the surface in the Skagerrak (Gustafsson, 1999; Bjo¨rk and Nordberg, 2003) and higher salinity North Sea and North Atlantic water at depth. The stability of the water stratification is variously enhanced by the influx of freshwater from ¨ rekils7lven at the head of the fjord, the the river O presence of sea-ice during cold winters and a small, semi-diurnal tidal range (0.15–0.30 m). The residence time of the low saline surface water is about 16–26 days and that down to the sill depth is about 40 days (Arneborg, 2004). Instrumental records demonstrate that the residence time of the surface waters has not changed between 1954 and 1986 and no decreasing or increasing trends have been recognised (Arneborg, 2004). The deeper more saline waters are relatively stagnant and are usually only exchanged during the winter or spring months when northerly to easterly winds induce upwelling due to Ekman pumping in the coastal waters (Rydberg, 1975). The deepest parts of the fjord, below 80 m, are occasionally subjected to hypoxic conditions during the autumn and winter as oxygen levels inevitably fall progressively throughout the year. However, since the late 1960s and early mid 1970s, it is accepted by the scientific community that Gullmar Fjord has not been subjected to any major source of water pollution from either sewage or industry (see later discussion). Before that, the inner part of the fjord received large amounts of oxygen-consuming substances from a paper mill, a sulphite mill (founded in the 1870s) and other anthropogenic activities (Rosenberg, 1990). In Lysekil, in the outer part of the fjord, untreated sewage and outlets from herring canneries ceased during the early 1970s. Nowadays it is acknowledged that there are no major sources of water
pollution from either sewage or industry within the environs of the fjord (Lindahl et al., 1998). In spite of this, and the closure of factories and the establishment of ambitious sewage treatment plants, little improvement has been noted in the quality of water from the fjord or indeed anywhere along the Swedish west coast. Therefore despite the lack of significant local sources of pollutants within the fjords, human induced eutrophication is still considered as ongoing and worsening (Rosenberg, 1990; Lindahl et al., 1998). Lately, however, this conventional wisdom has been challenged by research indicating a significant connection between the hydrography of the fjords on the Swedish west coast, with weather conditions/ climate on a decadal time scale, and larger scale marine pollution. In particular it has been demonstrated that variations in climate, in combination with the fjord morphology, has influenced the marine environment in respect to the frequency of water renewals in the fjords with the possible consequential establishment of stagnant bottom water, oxygen deficiency and benthic mortality (Nordberg et al., 2000, 2001). During the last 20 years or so the winters have been mild, humid and characterised by predominantly westerly winds (Bjo¨rk and Nordberg, 2003). This pattern has had a significant negative influence on both coastal and fjord environments with a marked decrease of renewal events. A major problem is, however, that the influence from human impact and the changes in the climate have acted almost simultaneously and thereby largely prevented the possibility of separating artificial and cultural effects from natural causes. Indeed recent research has suggested that there is a possible causal relationship between variations in the North Atlantic Oscillation (NAO) and the marine environment within Gullmar Fjord (Lindahl et al., 1998, 2003; Nordberg et al., 2000). In particular an indirect link between the NAO, the supply of nutrients and primary production has been suggested (Lindahl et al., 1998). This relationship has also been explored in an adjacent fjord, Koljo¨ Fjord, which is more restricted in its access to the Skagerrak than Gullmar Fjord (Harland et al., 2004a,b). Both fjords appear to react to the activity of the NAO in somewhat different ways
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seemingly as a direct consequence of their unique hydrography. The analysis of sediments deposited in Gullmar Fjord, and their contained foraminiferal faunas, have detailed a striking faunal change during the mid 1970s from a normal Skagerrak-Kattegat fauna to an opportunistic low oxygen fauna (Nordberg et al., 2000; Filipsson and Nordberg, 2004). Recent revisions to the dating of this event favour the year of 1979, which may relate to a widespread low oxygen event occurring in 1979/1980 (Filipsson and Nordberg, 2004). This appears to follow the change from negative winter NAO to positive winter NAO and the establishment of mild, humid winters and prevailing westerly winds. These westerly winds move low saline Baltic waters towards the coast (Gustafsson and Stigebrandt, 1996; Gustafsson, 1999), which lessens the frequency of upwelling events and the consequential exchange of bottom waters in the fjord so enhancing the depletion of oxygen (Nordberg et al., 2000; Bjo¨rk and Nordberg, 2003).
2. Historical note Gullmar Fjord is one of the most studied marine areas in the world with the first hydrographical measurements being taken as early as 1869. Indeed the Kristineberg Marine Research Station, one of the world’s oldest marine research stations, was founded in 1877 by the Royal Swedish Academy of Sciences at Fiskeb7ckskil on the shores of the fjord (Fig. 1). In 1954 Erdtman published one of the first studies, if not the first, on the occurrence of living dinoflagellate cysts, produced by the local phytoplankton, settling through the water column of the fjord over the years 1947 to 1949. The material was collected in bottomless corked flasks, fixed inverted 15 m below mean sea level and some 22 m from the shore. The flasks were changed monthly and the sediment analysed following treatment with hydrogen fluoride and acetolysis. The dinoflagellate cysts recovered were identified by Professor Trygve Braarud and figured in the consequent publication. The cysts include Protoceratium reticulatum (?Islandinium minutum) Fig. 1A; cf. Peridinium triquetrum (Protoceratium reticulatum) Fig. 1B; dnot a dinoflagellate cystT (?Spini-
207
ferites bentorii) Fig. 1C; dprobably a dinoflagellate cystT (?Spiniferites sp. indet.) Fig. 1D; dpart of a dinoflagellate cystT (?Incertae sedis) Fig. 2A; cf. Goniaulax polyedra (Lingulodinium polyedrum) Fig. 2B; Goniaulax polyedra (Lingulodinium polyedrum) Fig. 3A; and dprobably a dinoflagellate cystT (Protoceratium reticulatum) Fig. 4. The identifications provided in parentheses are our interpretations of the species illustrated by Erdtman (1954) with their modern epithets. It is interesting to note that in this early pioneering work the cysts collected were recognised as being viable and, therefore, not reworked and that they might prove useful in marine stratigraphy. Erdtman (1954, p. 110) asked bWill it be possible to use, to some extent at least, hystrichosphaerids and hystrichosphaeridoid organisms in the same way as pollen grains and spores in peats and lacustrine sediments? If this can be done, marine sediments poor in pollen grains or lacking them altogether, would, nevertheless, be accessible to micropalaeontological investigations similar to pollen statistics.Q In the context of our research, detailed herein, it is relevant to reiterate some of Erdtman (1954) original findings. In particular he noted that the dsporesT of Goniaulax polyedra (Lingulodinium polyedrum) were common in some samples especially in September and the first week in October when they were sixty-six times more frequent than the recovered pollen grains. In addition the palynological assemblages collected over this autumnal period were twice as large as those collected during the spring pollen maximum in May. Recent opportunistic research on the seasonal production of dinoflagellate cysts, as trapped within the flocculent layer (Harland et al., 2004b), from Koljo¨ Fjord is consistent with Erdtman’s earlier findings and confirms and identifies Lingulodinium polyedrum as a species that produces cysts towards the end of the summer and into the early autumn as also noted previously by Dale (1976) and Lewis and Hallett (1997). The relationship between planktonic dinoflagellates and cyst production in Gullmar Fjord has been explored rather more recently using sediment traps deployed for short three-day periods from the end of May to mid-June 1998 (Godhe et al., 2001). The seasonality of cyst production was demonstrated and the commonest species in the traps and plankton were
208
Core GA113–2Ab Dinoflagellate Cyst Analysis Analyst: R Harland
Peridiniacean and Protoperidin’ cysts
Gymnodinialean cysts
1985 -
0.10
1978 -
0.15
1971 -
0.20
1964 -
0.25
1957 1950 -
Depth (m)
0.05
YS i
LL
tzi
GE
ar
LA
hw
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IN
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TA TO
Po
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din no m Gy
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niu idi er op ot Pr
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m niu idi er op ot Pr
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nic co Pr
?P
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idi
ar
niu
so
m
din
ng elo es rit fe ini Sp
/n
es oid
lei ium
us at
ii or nt be es rit fe ini Sp
Pr
da
tu ula tic re ium at er oc ot
lod gu Lin
0.00 1992 -
Bi
te
cta
to
ini
din
um
ium
po
te
lye
pik
dr
a
ien
m
se
um
Gonyaulacacean cysts
Zone
CONISS
Unit I
Unit IIa
0.30 0.35
1942 -
0.40
1935 -
0.45
1928 -
0.50
1921 -
0.55
1914 -
0.60
Unit IIb
Unit IIc
100 200 300 400 0.65
1000 2000 3000
1000 2000 3000
100
200
300
50
100
150
100
200
300
20
40
60
80
100
100 200 300 400 500
1000 200030004000 5000
100 200 300 400
100 200 300 400
200040006000800010000
20000 40000 60000 80000 Total sum of squares
Fig. 2. Dinoflagellate cyst spectrum of selected species from Core GA113-2Ab, constructed using the cyst per gram data. The CONISS cluster analysis together with the visual inspection allows the core to be subdivided into the informal units as shown and described in the text. The 210Pb dating is indicated on the left of the figure.
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gullmar Fjord
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Pentapharsodinium dalei, related Scrippsiella spp. and Protoceratium reticulatum. Gonyaulax spinifera was absent from the plankton although some cysts were recovered from the sediment traps; Lingulodinium polyedrum was rarely observed in the plankton but was absent in the traps. Pentapharsodinium dalei is known as a spring blooming species in contrast to Lingulodinium polyedrum, which is well documented as favouring the late summer/autumn (see above). Godhe et al. (2001) found no linear relationship between cyst forming species in the plankton and the number of cysts in the traps. They also demonstrated, using multiple regression analysis, correlation with SST, ambient light radiation, and the halocline depth in contrast to the nutrient concentrations that appeared to correlate only poorly. It was noted that the dinoflagellates were undergoing sexual reproduction throughout the period of study and that temperature and light intensity appear to be of some importance in cyst formation. It is with this particular background that this new analysis of the dinoflagellate cysts from Gullmar Fjord was initiated as part of a larger study aimed at understanding the relationship between climate, hydrography and oxygen deficiency in bottom water from fjords along the west coast of Sweden. An analysis of the highresolution temporal record of the dinoflagellate cysts occurring in the latest Holocene sediments was, therefore, carried out to provide a proxy record for environmental change within the surface waters of the fjord. It was anticipated that comparison with results available from the restricted Koljo¨ Fjord would prove to be particularly useful to our understanding of the response of the west coast of Sweden to various changes both natural and cultural. In particular a primary aim of the study was to attempt to disentangle the effects of natural climatic fluctuations from cultural disturbances such as eutrophication and marine pollution. The analysis of dinoflagellate cysts is increasingly being used to document eutrophication and various aspects of marine pollution in coastal waters (Dale, 1996, 2001; Matsuoka, 1999, 2001; Pospelova et al., 2002, 2004; Sangiorgi and Donders, 2004) with much of this discussion published within the pages of The Science of the Total Environment.
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3. Materials and methods 3.1. Sampling and processing The sediment core site G113, situated at Lat: 588 18V95 N and Long: 118 32V36 E (Fig. 1) was sampled by several cores taken in June 1999 by the r/v Skagerak using a Gemini Corer. This method of core collection provides a virtually undisturbed sediment/water interface and a core some 80 mm in diameter and 610 mm in length. After collection the cores were X-rayed on board ship with an Andrex BV (155 140 Kv/5mA) portable machine before further investigation. In the laboratory the cores were sliced and analysed for their organic carbon content using a Carlo Erba NA 1500 instrument. Radiometric dating using the 210Pb methodology and the constant rate of supply (CRS) model of Appleby and Oldfield (1978) was carried out at the Department of Radiation Physics, University of Lund, Sweden on one of the cores, GA113-1A, (see Nordberg et al. (2001) and Filipsson and Nordberg (2004) for further details and the age depth profile). A correlation with the core analysed herein, GA113-2Ab, was effected using foraminiferal marker levels and in particular the marked increase in the proportions of the opportunistic foraminifera Stainforthia fusiformis (Williamson). The sediment accumulation rate was calculated at 0.7 cm/year and the dating is indicated on the dinoflagellate cyst spectrum (Fig. 2). A suite of sixty samples was taken from the recovered core GA113-2Ab, (the original core GA113-2A was split so that one half, GA1132Aa, was analysed for foraminifera whereas the second, GA113-2Ab, was analysed for both diatoms (see McQuoid and Nordberg, 2003) and dinoflagellate cysts), at a sample interval of 1 cm and, therefore, encompassing some 60 cm of sediment. The sediment is homogenous, organicrich clay (Nordberg et al., 2000) and it is estimated from the 210Pb radiometric dating study on core GA113-1A that the suite of samples represents a time interval from 1915 until 1999. All the samples were processed to extract the dinoflagellate cysts using the normal palynological processing techniques as described by Wood et al. (1996). In
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particular the samples were treated consistently throughout to maintain the integrity of the dataset. The samples were not subjected to any oxidising reagents to prevent the differential loss of protoperidiniacean cysts (Dale, 1976; Zonneveld et al., 1997) but were subjected to prolonged washing and filtering together with the use of ultrasound, up to 2 min, to free the dinoflagellate cysts from the amorphous organic material (AOM) that is always present in these nearshore fjord samples. The resulting palynological residues were stained with Safranin and dispersed onto microscopical coverslips using Elvacite and bonded to slides using Petrapoxy 154 resin, which has a refractive index of 1.54. In addition the samples were treated quantitatively so that the numbers of cysts per gram of sediment could be calculated. The original dry weight of sediment was noted; usually 5 g in this instance, and aliquot subsamples of the organic residues were taken for mounting and counting (Harland, 1989). Samples were counted on a single slide, representing either 1 g of original sediment or a fraction thereof, with a 40 objective using a Zeiss Axiolab microscope. The derived data are detailed in Tables 1 and 2 and include the raw counts and the calculated number of cysts per gram of sediment, respectively. TILIA/TILIAGRAPH software has been used to construct a dinoflagellate cyst spectrum and Fig. 2 illustrates the spectrum based upon certain selected species. A full taxonomic listing of the recovered cysts can be found in the short systematic section to this contribution. 3.2. Data treatment 3.2.1. Dinoflagellate cysts Stratigraphically constrained incremental sum of squares cluster analysis using CONISS (Grimm, 1987) as part of the software package has also been employed in the analysis of the dinoflagellate cyst assemblages to differentiate the various assemblages through the core and to assist in the visual interpretation of the diagram, and a heterotrophic ratio was calculated from the numbers of dinoflagellate cysts present within the samples (Powell et al., 1990; Dale, 1996). This heterotrophic ratio is simply the numbers of cysts from heterotrophic dinoflagellates divided by
those identified as derived from autotrophic dinoflagellates and expressed as a log value (Fig. 3). The first use of such a ratio to express differences within the cyst assemblages was published by Harland (1973) who recognised the different apparent ecological requirements of gonyaulacacean and peridiniacean cysts from their distributions in modern sediments as known at the time (Wall and Dale, 1968); this was later expressed and explained as fundamental differences in trophic behaviour (Harland, 1988). The trophic assignment of the various species is provided in the taxonomic listing. High values of the ratio are indicative of the greater presence of the cysts of heterotrophic dinoflagellates. Relative increases of heterotrophic dinoflagellates, as evidenced by their cyst production, have been used to indicate the increased presence of their prey species. This has been assumed to indicate the probable enhancement of nutrients as the phenomenon has been linked to areas of upwelling (see Powell et al., 1990, etc.). Heterotrophic dinoflagellates often prey upon diatoms as a first choice and, therefore, as diatom numbers rise, in response to increased nutrient supply, the heterotrophic dinoflagellate populations follow; the fundamental assumption is that this effect produces a higher cyst yield. However apparent increases in the proportions of heterotrophic dinoflagellates can also be caused by a decrease in the proportions of autotrophic dinoflagellate cysts; it is often difficult, if not almost impossible, to disentangle this phenomenon (see discussion). Unfortunately for the moment there is no research available that securely links these phenomena into a coherent picture much less providing a model that can be used for palaeoecological interpretations. It is, therefore, advisable to treat the use of the heterotrophic ratio as a guide only and with a significant amount of caution until a model is available based with confidence upon modern data. 3.2.2. Hydrographic and atmospheric data In order to compare the data from different instrumental records with the dinoflagellate cyst record the data sets had to be treated differently, especially with respect to averaging over time, as the sampling density between them varied. All the surface water data was, however, depth averaged between 0–10 m. We present this yearly hydro-
Table 1 Dinoflagellate cyst analysis as raw counts Gullmar Fjord, Sweden Core GA113-2Ab Raw counts
RH414 RH415 RH416 RH417 RH418 RH419 RH420 RH421 RH422 RH423 RH424 RH425 RH426 RH427 RH428 RH429 RH430 RH431 RH432 RH433 0.01 m 0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09
0.1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19
0.2
0 4 2 0 64 7 0 0 0 0 0 9
0 2 6 0 64 0 0 3 0 0 0 9
0 3 12 0 41 0 0 0 0 0 0 3
0 5 0 0 49 4 0 1 0 0 0 9
0 0 0 0 62 3 0 1 0 0 0 8
1 0 4 0 53 3 0 0 0 0 0 10
0 0 6 0 33 1 0 1 0 0 1 5
0 0 0 0 36 3 0 5 0 0 1 11
0 0 5 0 75 5 1 0 0 0 0 14
0 2 0 0 103 6 0 1 0 0 0 9
1 0 1 0 55 5 0 2 0 0 0 10
0 0 2 0 43 9 0 2 0 0 0 10
0 0 7 0 57 3 0 1 0 0 2 9
0 1 1 0 41 10 0 0 0 0 0 18
2 0 0 0 33 15 0 1 0 0 1 13
0 1 13 0 60 13 1 2 0 0 2 19
0 1 11 0 41 7 0 2 0 1 0 17
0 3 21 0 31 10 2 3 0 0 0 13
0 2 11 0 59 2 0 0 0 0 0 7
2
0
4
5
14
4
6
12
11
2
5
0
2
0
0
3
3
3
2
2 0 0 1 0 3 9 0 0 3 3 3 0 0 1 132 0
3 0 0 2 0 0 5 0 0 0 0 0 3 0 0 112 1
9 0 0 0 0 6 11 0 0 1 3 2 0 1 0 131 3
41 0 1 1 3 3 15 0 0 1 2 0 1 0 0 251 6
28 0 1 0 0 3 23 0 1 0 6 1 0 0 0 251 4
13 0 0 0 1 5 11 0 0 2 4 0 0 0 0 156 4
7 0 1 0 0 0 6 0 0 1 3 0 0 0 0 84 1
6 0 0 0 0 4 15 0 0 0 3 1 0 0 0 96 2
3 0 0 0 0 6 10 1 0 0 2 1 0 1 0 119 4
1 0 1 0 0 2 9 0 0 2 2 0 0 0 0 128 6
9 0 0 0 1 13 9 0 1 1 2 0 1 0 0 174 1
1 0 0 0 0 1 7 0 0 0 5 1 2 0 0 102 3
7 0 0 0 0 5 25 0 0 3 2 2 1 0 2 157 4
2 0 3 0 0 1 14 0 0 3 3 0 0 0 0 164 6
3 0 4 0 2 0 19 0 1 1 7 1 3 0 0 186 7
3 0 3 0 0 2 16 0 1 1 4 0 1 2 0 136 3
4 0 0 0 3 2 10 0 0 0 0 0 1 0 0 99 4
4 0 0 0 0 1 6 0 1 1 0 0 0 0 0 66 0
0 0 0 0 0 0 9 0 0 3 0 0 0 0 0 84 3
0 5 8 257
0 2 3 221
0 12 6 248
0 21 8 427
0 4 9 419
0 2 8 281
0 5 4 165
0 11 13 219
0 10 7 275
0 10 9 293
0 11 14 316
0 9 2 199
0 9 8 306
0 11 19 297
0 9 17 328
0 5 10 301
0 4 15 225
0 0 23 188
0 5 5 192
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane 0 Bitectatodinium tepikiense 0 Lingulodinium polyedrum 1 Nematosphaeropsis labyrinthus 0 Protoceratium reticulatum 8 Spiniferites bentorii 4 Spiniferites delicatus 0 Spiniferites elongatus 0 Spiniferites lazus 0 Spiniferites mirabilis 0 Spiniferites ramosus 0 Spiniferites spp. indet. 9 Peridiniacean cysts ?Pentapharsodinium dalei 0 Protoperidiniacean cysts Islandinium cf. cesare 1 Lejeunecysta marieae 0 Lejeunecysta oliva 0 Protoperidinium avellana 0 Protoperidinium claudicans 0 Protoperidinium conicoides 5 Protoperidinium conicum/nudum 12 Protoperidinium compressum 0 Protoperidinium divaricatum 0 Protoperidinium leonis 1 Protoperidinium oblongum 1 Protoperidinium pentagonum 0 Protoperidinium punctulatum 0 Protoperidinium subinerme 0 Protoperidinium spp. indet. [P] 0 Protoperidinium spp. indet. [RB] 104 Protoperidinium sp. nov. 0 Gymnodinialean cysts Cyst nov. [sparse spiny] 0 Gymnodinium catenatum 6 Polykrikos schwartzii 5 n 157
(continued on next page)
211
212
Table 1 (continued) Gullmar Fjord, Sweden Core GA113-2Ab
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts ?Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spiny] Gymnodinium catenatum Polykrikos schwartzii
RH434 RH435 RH436 RH437 RH438 RH439 RH440 RH441 RH442 RH443 RH444 RH445 RH446 RH447 RH448 RH449 RH450 RH451 RH452 RH453 0.21
0.22
0.23
0.24
0.25
0.26
0.27
0.28
0.29
0.3
0.31
0.32
0.33
0.34
0.35
0.36
0.37
0.38
0.39
0.4
0 1 59 1 109 9 0 1 0 0 0 25
0 2 45 0 35 2 0 0 0 0 1 16
0 0 26 0 32 2 3 0 0 1 0 13
0 1 37 0 52 9 2 3 0 3 0 10
0 2 93 1 58 3 0 0 0 5 2 18
0 2 65 0 44 6 0 3 0 2 2 16
0 0 34 0 55 4 0 4 0 0 1 12
0 1 88 0 75 6 0 3 0 2 3 19
0 7 62 0 50 6 0 1 0 1 0 16
0 0 54 0 49 4 0 1 0 0 0 16
0 0 96 0 71 2 0 5 0 3 0 13
1 7 77 0 107 8 0 5 0 0 1 32
0 6 112 0 70 2 0 2 0 1 0 28
0 3 73 0 52 1 1 5 0 0 0 16
0 9 119 0 75 5 4 2 0 1 0 30
0 4 118 0 69 7 1 1 0 0 0 20
0 2 97 0 66 5 0 9 0 0 0 30
0 11 124 0 71 4 1 5 0 2 0 29
0 5 69 0 54 5 0 1 0 0 0 17
0 10 166 0 90 7 0 8 0 2 0 36
3
4
1
0
8
13
0
0
0
0
0
0
0
0
0
0
1
2
1
2
12 0 0 0 0 0 9 0 0 0 2 0 0 0 0 192 1
4 0 0 0 0 0 2 0 0 1 0 0 0 0 0 61 4
1 0 0 0 0 1 6 0 0 0 0 0 0 0 0 60 2
4 0 0 0 0 2 8 0 0 0 2 0 0 0 0 89 1
8 0 1 0 0 0 5 0 0 3 2 1 0 0 0 74 2
3 0 0 0 1 0 6 0 0 2 5 0 1 0 0 71 1
3 0 0 0 0 2 13 0 0 0 1 0 3 1 0 62 0
4 0 1 0 0 1 14 0 0 2 4 0 0 1 0 86 0
1 0 0 0 1 0 9 0 1 0 2 1 0 0 1 56 1
4 0 0 0 0 0 8 2 0 1 1 0 1 0 2 54 0
5 0 1 0 0 0 7 0 1 0 1 0 0 0 2 69 1
1 0 1 0 0 0 19 1 0 0 3 0 1 0 3 119 1
2 0 3 0 2 0 7 2 0 1 0 0 0 0 1 70 1
2 0 1 0 0 0 11 1 0 0 0 0 0 0 0 44 1
0 0 0 0 0 0 14 0 0 1 1 1 0 3 4 69 0
0 0 0 0 1 0 17 1 0 0 1 0 0 0 2 89 2
1 0 0 0 0 1 14 0 1 2 0 0 0 0 2 88 0
1 0 0 0 0 0 18 1 1 3 1 0 0 0 5 91 1
0 0 2 0 0 0 8 0 0 1 2 0 2 0 0 76 1
4 0 1 0 0 0 11 0 0 3 5 1 0 0 9 103 1
0 12 22
0 2 5
0 1 5
0 0 8
0 4 12
0 0 10
0 3 2
0 7 7
0 0 5
0 2 2
0 3 5
0 6 1
0 4 3
0 3 1
0 6 2
0 9 2
0 8 6
0 6 2
0 10 2
0 3 1
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Raw counts
Gullmar Fjord, Sweden Core GA113-2Ab Raw counts
0.42
0.43
0.44
0.45
0.46
0.47
0.48
0.49
0.5
0.51
0.52
0.53
0.54
0.55
0.56
0.57
0.58
0.59
0.6
0 10 108 0 60 4 0 2 0 0 4 22
0 4 94 0 86 2 0 4 0 8 0 15
0 14 107 0 140 1 0 3 0 0 3 29
0 8 89 0 96 5 0 3 0 2 0 24
1 6 149 0 118 6 1 4 0 1 0 23
0 2 92 0 70 3 1 2 1 0 0 17
0 10 146 0 120 3 0 7 0 3 0 30
0 10 151 0 108 5 0 3 0 0 0 27
0 3 136 0 90 4 3 2 2 0 0 38
0 3 90 0 110 0 3 1 0 0 0 24
0 9 44 0 117 0 0 0 0 0 0 30
0 3 34 0 78 1 1 1 0 0 0 19
0 12 49 0 89 0 1 1 0 1 0 13
0 5 26 0 85 0 0 2 0 0 0 11
0 23 28 0 125 3 2 5 0 0 1 25
0 5 20 0 52 2 0 1 0 0 0 8
0 6 14 0 92 0 1 0 0 2 0 20
0 6 35 0 119 0 1 3 0 3 0 21
0 9 24 0 69 0 0 2 0 4 0 14
0 6 16 0 87 1 1 4 0 0 0 17
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
5 0 0 0 2 0 9 0 0 0 4 0 0 0 6 77 1
3 0 2 0 0 0 4 0 1 2 4 0 2 2 6 122 19
7 0 0 0 0 2 15 0 2 0 4 0 0 1 2 144 1
0 0 0 0 1 0 7 0 0 0 0 0 0 0 7 99 0
7 0 0 0 2 1 10 0 0 1 6 0 0 1 3 134 3
7 0 1 0 0 0 9 1 0 0 1 0 0 1 1 110 0
4 0 1 0 0 1 14 0 0 0 4 1 1 0 3 145 0
4 0 4 0 2 0 15 0 0 1 0 0 0 0 3 156 0
9 0 3 0 0 0 10 0 1 0 3 0 0 0 2 157 0
5 0 2 0 0 4 13 0 0 1 3 0 0 1 3 148 0
16 0 2 0 0 3 26 1 0 2 3 0 0 0 0 170 0
8 0 1 0 1 4 29 0 0 0 0 0 0 1 1 150 0
7 0 0 0 0 1 24 0 0 1 2 0 0 1 3 168 0
5 0 0 0 2 6 5 0 2 0 0 0 1 1 2 114 0
5 1 3 0 2 0 9 0 3 0 4 0 0 0 1 148 0
6 0 2 0 0 3 4 0 1 0 1 0 0 0 1 62 0
7 1 3 0 1 6 9 0 1 0 2 1 0 0 0 142 3
11 0 1 0 2 4 13 0 1 0 5 0 0 0 0 146 0
3 0 0 0 0 0 5 0 0 0 4 1 0 0 3 65 1
4 0 2 0 0 4 7 0 0 0 2 0 1 1 2 90 0
0 6 8 328
0 8 3 386
0 19 8 502
0 12 4 357
0 24 5 506
0 5 7 331
0 13 5 511
0 6 3 498
0 11 3 477
0 14 2 427
0 18 4 445
0 11 5 348
0 20 4 397
2 9 9 291
9 17 10 424
1 10 1 180
4 14 1 330
5 18 6 400
0 11 1 216
0 11 3 259
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts ?Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spiny] Gymnodinium catenatum Polykrikos schwartzii n
RH454 RH455 RH456 RH457 RH458 RH459 RH460 RH461 RH462 RH463 RH464 RH465 RH466 RH467 RH468 RH469 RH470 RH471 RH472 RH473 0.41
213
214
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
graphical data in Figs. 3 and 6, but the larger part of the data sets were divided into two periods, a spring period (March, April and May) and a late summer–autumn (July, August and September) (Figs. 4 and 5). 3.2.2.1. Alsba¨ck series. Despite the Alsb7ck data being the longest period of monitoring for the area there are gaps in the data set. During the early part of the 20th century, salinity and temperature were measured intermittently and it was not until 1958 that measurements became more frequent and dissolved inorganic phosphate (PO4-P) became one of the measured variables. During the late 1960s and in the 1970s dissolved inorganic nitrogen (DIN, sum of NO3, NO2 and NH4) also started to be monitored and in 1980 the measuring frequency became monthly. Unfortunately since 1991 no measurements are taken on the surface water of the fjord within the monitoring programme of this station. This contribution presents all temperature and salinity data for the spring, and late summer– autumn periods, between the years 1890 and 1991 but the data were not averaged because of the varying measuring frequencies. Also presented are the available data sets for PO4 and DIN. The location of the monitoring station is indicated in Fig. 1. These data are available from the Swedish Meteorological and Hydrological Institute (SMHI) and the Water Quality Association of the Bohus Coast (BVVF); hydrographic data before 1958 are from Engstro¨m (1970). 3.2.2.2. Borno¨ series. The Borno¨ series is a unique data set for the Swedish west coast, consisting of daily measurements between the years 1931 and 1989, except Sundays and holidays, of salinity and temperature from eight depths within the water column of Gullmar Fjord. Since the data set is so densely sampled the averages have been calculated for both the spring and late summer/autumn time periods. Further details of this remarkable data series are published in Bjo¨rk and Nordberg (2003) and Arneborg (2004). The location of the Borno¨ sampling station is indicated in Fig. 1. 3.2.2.3. Upwelling events. The upwelling events were calculated using geostrophic wind data. The upwell-
ing event series (Figs. 3–5) was supplied by Bjo¨rk and Nordberg (2003) who should also be consulted for details of their data handling and calculations. 3.2.2.4. Air temperature and precipitation data from Vinga Island. Vinga Island is situated some 10 km west of Go¨teborg (Fig. 1) and air temperature and precipitation were measured daily from 1860 (temperature) and 1879 (precipitation) until 1997 when the station was closed. We present the temperature averages over March to May and July to September (Figs. 4 and 5) and annual precipitation between the years 1890 and 1997, together with the annual precipitation data from Lysekil, between the years 1973 and 2000 (Fig. 3). 3.2.2.5. NAO index. The North Atlantic Oscillation (NAO) has a pronounced effect on the winter climate in Scandinavia (Chen and Hellstro¨ m, 1999). To quantify the NAO, a simple pressure index can be derived from the normalized sea level pressure difference between the Icelandic low and the Azores high (Hurrell, 1995). The NAO index provided herein is the same as that presented by Hurrell (1995) and on the web page http:// www.cgd.ucar.edu/~jhurrell/nao.stat.other.html. The index is averaged over the three winter months January to March and is presented together with a three year running mean (Fig. 3). 3.2.2.6. Primary productivity. Primary productivity is shown in Fig. 6, and has been measured in the fjord using both the 14C technique and the chlorophyll a concentrations. The 14C measurements were taken at Sl7ggo¨, towards the mouth of the fjord (Fig. 1) and the chlorophyll a measurements were taken from the inner part of the fjord (Fig. 1). The 14C data is redrawn from Lindahl et al. (2003); details regarding the 14C method are provided in Lindahl et al. (1998, 2003). The chlorophyll a data are from the Swedish Meteorological and Hydrological Institute (SMHI) and Water Quality Association of the Bohus Coast (BVVF).
4. Results Dinoflagellate cysts were recovered from all the sampled horizons throughout the uppermost 60 cm of
Table 2 Dinoflagellate cyst analysis as calculated cysts per gram of sediment Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09
0.1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19
0.2
0.21
0 0 6 0 51 26 0 0 0 0 0 58
0 64 32 0 1024 112 0 0 0 0 0 144
0 32 96 0 1024 0 0 48 0 0 0 144
0 48 192 0 656 16 0 0 0 0 0 48
0 80 0 0 784 64 0 16 0 0 0 144
0 0 0 0 992 48 0 16 0 0 0 128
16 0 64 0 848 48 0 0 0 0 0 160
0 0 96 0 528 16 0 16 0 0 16 80
0 0 0 0 576 48 0 80 0 0 16 176
0 0 80 0 1200 80 16 0 0 0 0 224
0 32 0 0 1648 96 0 16 0 0 0 144
16 0 16 0 880 80 0 32 0 0 0 160
0 0 32 0 688 144 0 32 0 0 0 160
0 0 112 0 912 48 0 16 0 0 32 144
0 16 16 0 656 160 0 0 0 0 0 288
32 0 0 0 528 240 0 16 0 0 16 208
0 16 208 0 960 208 16 32 0 0 32 304
0 16 176 0 656 112 0 32 0 16 0 272
0 48 336 0 496 160 32 48 0 0 0 208
0 32 176 0 944 32 0 0 0 0 0 112
0 16 944 16 1744 144 0 16 0 0 0 400
0
32
0
64
80
224
64
96
192
176
32
80
0
32
0
0
48
48
48
32
48
6 0 0 0 0 32 77 0 0 6 6 0 0 0 0 666 0
32 0 0 16 0 48 144 0 0 48 48 48 0 0 0 2112 0
48 0 0 32 0 0 160 0 0 0 0 0 48 0 0 1792 32
144 0 4 0 0 96 176 0 0 16 48 32 0 16 0 2096 48
656 0 16 16 48 48 240 8 0 16 32 0 16 0 0 4016 120
448 0 16 0 0 48 368 0 16 0 96 16 0 0 0 4016 64
208 0 0 0 16 80 176 0 0 32 64 0 0 0 0 2496 64
112 0 16 0 0 0 80 0 0 16 48 0 0 0 0 1344 16
96 0 0 0 0 64 240 0 0 0 48 16 0 0 0 1536 32
48 0 0 0 0 96 160 16 0 0 32 16 0 16 0 1904 64
16 0 16 0 0 32 144 0 0 32 32 0 0 0 0 2048 96
144 0 0 0 16 80 272 0 16 16 32 0 16 0 0 2784 16
16 0 0 0 0 16 112 0 0 0 80 16 32 0 0 1632 48
112 0 0 0 0 80 400 0 0 48 32 32 16 0 32 2512 64
32 0 48 0 0 16 224 0 0 48 48 0 0 0 0 2624 96
48 0 64 0 32 0 304 0 16 16 112 16 48 0 0 2976 112
48 0 48 0 0 32 256 0 16 16 64 0 16 32 0 2176 48
64 0 0 0 48 32 164 0 0 0 0 0 16 0 0 1584 64
64 0 0 0 0 32 96 0 16 16 0 0 0 0 0 1056 0
0 0 0 0 0 0 144 0 0 48 0 0 0 0 0 1344 48
192 0 0 0 0 0 144 0 0 0 32 0 0 0 0 3072 16
0 38 32 1005 141 787 5.58 0.75
0 80 128 4112 1408 2464 1.75 0.24
0 32 48 3536 1344 2064 1.54 0.19
0 192 96 3968 1024 2532 2.47 0.39
0 336 128 6832 1168 4576 3.92 0.59
0 64 144 6704 1408 4640 3.30 0.52
0 32 128 4496 1200 2928 2.44 0.39
0 80 64 2640 848 1520 1.79 0.25
0 176 208 3504 1088 1936 1.78 0.25
0 160 112 4400 1776 2304 1.30 0.11
0 160 144 4688 1968 2400 1.22 0.09
0 176 224 5056 1264 3248 2.57 0.41
0 144 32 3184 1056 1936 1.83 0.26
0 144 128 4896 1296 3216 2.48 0.39
0 176 304 4752 1136 3104 2.73 0.44
0 144 272 5248 1040 3696 3.55 0.55
0 80 160 4816 1824 2704 1.48 0.17
0 64 240 3600 1328 1908 1.44 0.16
0 0 368 3008 1376 1216 0.88 0.05
0 80 80 3072 1328 1584 1.19 0.08
0 192 352 7328 3328 3264 0.98 0.01
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio Log H:A Ratio
RH414 RH415 RH416 RH417 RH418 RH419 RH420 RH421 RH422 RH423 RH424 RH425 RH426 RH427 RH428 RH429 RH430 RH431 RH432 RH433 RH434 0.01 m
(continued on next page)
215
216
Table 2 (continued) Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
0.23
0.24
0.25
0.26
0.27
0.28
0.29
0.3
0.31
0.32
0.33
0.34
0.35
0.36
0.37
0.38
0.39
0.4
0.41
0.42
0 32 720 0 560 32 0 0 0 0 16 256
0 0 416 0 512 32 48 0 0 16 0 208
0 16 592 0 832 144 32 48 0 48 0 160
0 32 1488 16 928 48 0 0 0 80 32 288
0 32 1040 0 704 96 0 48 0 32 32 256
0 0 544 0 880 64 0 64 0 0 16 192
0 16 1408 0 1200 96 0 48 0 32 48 304
0 112 992 0 800 0 0 16 0 16 0 256
0 0 864 0 784 64 0 16 0 0 0 256
0 0 1536 0 1136 32 0 80 0 48 0 208
16 112 1232 0 1712 128 0 80 0 0 16 512
0 96 1792 0 1120 32 0 32 0 16 0 448
0 48 1168 0 832 16 16 80 0 0 0 256
0 144 1904 0 1200 80 64 32 0 16 0 480
0 64 1888 0 1104 112 16 16 0 0 0 320
0 32 1552 0 1056 80 0 144 0 0 0 480
0 176 1984 0 1136 64 16 80 0 32 0 464
0 80 1104 0 864 80 0 16 0 0 0 272
0 160 2656 0 1440 112 0 128 0 32 0 576
0 160 1728 0 960 64 0 32 0 0 64 352
0 64 1504 0 1376 32 0 64 0 64 0 240
64
16
0
128
208
0
0
0
0
0
0
0
0
0
0
16
32
16
32
0
0
64 0 0 0 0 0 32 0 0 16 0 0 0 0 0 976 64
16 0 0 0 0 16 96 0 0 0 0 0 0 0 0 960 32
64 0 0 0 0 32 128 0 0 0 32 0 0 0 0 1424 16
128 0 16 0 0 0 80 0 0 48 32 16 0 0 0 1184 32
48 0 0 0 16 0 96 0 0 32 80 0 16 0 0 1136 16
48 0 0 0 0 32 208 0 0 0 16 0 48 16 0 992 0
64 0 16 0 0 16 224 0 0 32 64 0 0 16 0 1376 0
16 0 0 0 16 0 144 0 16 0 32 16 0 0 16 896 16
64 0 0 0 0 0 128 32 0 16 16 0 16 0 32 864 0
80 0 16 0 0 0 112 0 16 0 16 0 0 0 32 1104 16
16 0 16 0 0 0 304 16 0 0 48 0 16 0 48 1904 16
32 0 48 0 32 0 112 32 0 16 0 0 0 0 16 1120 16
32 0 16 0 0 0 176 16 0 0 0 0 0 0 0 704 16
0 0 0 0 0 0 224 0 0 16 16 16 0 48 64 1104 0
0 0 0 0 16 0 272 16 0 0 16 0 0 0 32 1424 32
16 0 0 0 0 16 224 0 16 32 0 0 0 0 32 1408 0
16 0 0 0 0 0 288 16 16 48 16 0 0 0 80 1456 16
0 0 32 0 0 0 128 0 0 16 32 0 32 0 0 1216 16
64 0 16 0 0 0 176 0 0 48 80 16 0 0 144 1648 16
80 0 0 0 32 0 144 0 0 0 64 0 0 0 96 1232 16
48 0 32 0 0 0 304 0 16 32 64 0 32 32 48 1952 96
0 32 80 2944 1680 1088 0.65
0 16 80 2464 1248 1104 0.88
0 0 128 3696 1872 1632 0.87
0 64 192 4832 3040 1408 0.46
0 0 160 4048 2448 1392 0.57
0 48 32 3200 1760 1312 0.75
0 112 112 5184 3152 1744 0.55
0 0 80 3440 2192 1152 0.53
0 32 32 3216 1984 1104 0.56
0 48 80 4560 3040 1312 0.43
0 96 16 6304 3808 2368 0.62
0 64 48 5072 3536 1392 0.39
0 48 16 3440 2416 928 0.38
0 96 32 5536 3920 1488 0.38
0 144 32 5504 3520 1808 0.51
0 128 96 5328 3360 1728 0.51
0 96 32 6064 3984 1936 0.49
0 160 32 4096 2432 1472 0.61
0 48 16 7408 5136 2144 0.42
0 96 128 5248 3360 1584 0.47
0 128 48 6176 3344 2608 0.78
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio
RH435 RH436 RH437 RH438 RH439 RH440 RH441 RH442 RH443 RH444 RH445 RH446 RH447 RH448 RH449 RH450 RH451 RH452 RH453 RH454 RH455 0.22
Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
RH457
RH458
RH459
RH460
RH461
RH462
RH463
RH464
RH465
RH466
RH467
RH468
RH469
RH470
RH471
RH472
RH473
0.44
0.45
0.46
0.47
0.48
0.49
0.5
0.51
0.52
0.53
0.54
0.55
0.56
0.57
0.58
0.59
0.6
0 224 1712 0 2240 16 0 48 0 0 48 464
0 128 1424 0 1536 80 0 48 0 32 0 400
16 96 2384 0 1888 96 16 64 0 16 0 368
0 32 1472 0 1120 48 16 32 16 0 0 272
0 160 2336 0 1920 48 0 112 0 48 0 480
0 160 2416 0 1728 80 0 48 0 0 0 432
0 48 2176 0 1440 64 48 32 32 0 0 608
0 48 1440 0 1760 0 48 16 0 0 0 384
0 144 704 0 1872 0 0 0 0 0 0 480
0 48 544 0 1248 16 16 16 0 0 0 304
0 192 784 0 1424 0 16 16 0 16 0 208
0 80 416 0 1360 0 0 32 0 0 0 176
0 368 448 0 2000 48 32 80 0 0 16 400
0 80 320 0 832 32 0 16 0 0 0 128
0 96 224 0 1472 0 16 0 0 32 0 320
0 96 560 0 1904 0 16 48 0 48 0 336
0 144 384 0 1104 0 0 32 0 64 0 224
0 96 256 0 1392 16 16 64 0 0 0 272
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
112 0 0 0 0 32 240 0 32 0 64 0 0 16 32 2304 16
0 0 0 0 16 0 112 0 0 0 0 0 0 0 112 1584 0
112 0 0 0 32 16 160 0 0 16 96 0 0 16 48 2144 48
112 0 16 0 0 0 144 16 0 0 16 0 0 16 16 1760 0
64 0 16 0 0 16 224 0 0 0 64 16 16 0 48 2320 0
64 0 64 0 32 0 240 0 0 16 0 0 0 0 48 2496 0
144 0 48 0 0 0 160 0 16 0 48 0 0 0 32 2512 0
80 0 32 0 0 64 208 0 0 16 48 0 0 16 48 2368 0
256 0 32 0 0 48 416 16 0 32 48 0 0 0 0 2720 0
128 0 16 0 16 64 464 0 0 0 0 0 0 16 16 2400 0
112 0 0 0 0 16 384 0 0 16 32 0 0 16 48 2688 0
80 0 0 0 32 96 80 0 32 0 0 0 16 16 32 1824 0
80 16 48 0 32 0 144 0 48 0 64 0 0 0 16 2368 0
96 0 32 0 0 48 64 0 16 0 16 0 0 0 16 992 0
112 16 48 0 16 96 144 0 16 0 32 16 0 0 0 2272 32
176 0 16 0 32 64 208 0 16 0 80 0 0 0 0 2336 0
16 0 0 0 0 0 80 0 0 0 64 16 0 0 48 1040 16
64 0 32 0 0 64 112 0 0 0 32 0 16 16 32 1440 0
0 304 128 8032 4752 2736 0.58 0.24
0 192 64 5712 3648 1824 0.50 0.30
0 384 80 8096 4944 2576 0.52 0.28
0 80 112 5296 3008 1984 0.66 0.18
0 208 80 8176 5104 2720 0.53 0.27
0 96 48 7968 4864 2896 0.60 0.23
0 176 48 7632 4448 2816 0.63 0.20
0 224 32 6832 3696 2800 0.76 0.12
0 288 64 7120 3200 3312 1.04 0.01
0 176 80 5568 2192 2992 1.36 0.14
0 320 64 6352 2656 3200 1.20 0.08
96 144 144 4656 2064 2224 1.08 0.03
144 272 160 6784 3392 2880 0.85 0.07
16 160 16 2880 1408 1200 0.85 0.07
80 224 16 5280 2160 2768 1.28 0.11
80 288 96 6400 3008 2832 0.94 0.03
0 176 16 3424 1952 1264 0.65 0.19
0 176 48 4144 2112 1744 0.83 0.08
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio Log H:A Ratio
RH456 0.43
217
218
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Core GA113-2Ab. The quantitative data are provided in Tables 1 and 2. In addition the samples contained bisaccate and angiosperm pollen together with copepod egg cases, foraminiferal linings and much structured and amorphous organic material. The numerical data, in particular the numbers of cysts per gram of sediment of selected species, have been used to construct the dinoflagellate cyst spectrum illustrated in Fig. 2. The cyst spectrum clearly demonstrates a number of features that are of note. Firstly it can be seen that the dinoflagellate cysts are well represented throughout the core, generally occurring at about the 4000 cysts per gram level but sometimes rising to over 7000 cysts per gram of sediment. These figures are much higher than those recorded for sediments preserved in Koljo¨ Fjord (Harland et al., 2004a) but are reasonably close to the figure recorded by Persson et al. (2000) of 11,000 from Alsb7ck, Gullmar Fjord. It is also clear that the Gullmar Fjord sediments contain higher numbers of gonyaulacacean cysts (up to 5000 cyst per gram) than those in neighbouring Koljo¨ Fjord (no more than 2000 cysts per gram), which undoubtedly reflects the more restricted nature of the water mass in the latter fjord. Indeed the fact that the accumulation rate in Gullmar Fjord is at least twice that in Koljo¨ Fjord (0.6–1.4 cm y 1 as opposed to 0.4 cm y 1) (Filipsson and Nordberg, 2004 and Nordberg et al., 2001), further accentuates the difference. It is interesting to note the presence of Ataxiodinium choane, Bitectatodinium tepikiense, Nematosphaeripsis labyrinthus, Protoceratium reticulatum and Spiniferites mirabilis within the Gullmar Fjord dataset, in contrast to Koljo¨ Fjord, as possible indicators of more open marine environments. Indeed all these species are known to occur in the Zone 1 assemblage of Dale (1985) of a core taken in the Skagerrak, which is also comparable with the present day cyst flora from the coastal waters of southern and western Norway (Grøsfjeld and Harland, 2001). In many respects the cyst spectrum from Gullmar Fjord is much less variable than that of Koljo¨ Fjord, in both cyst numbers and the record of individual cyst species, and consequently allows for less differentiation. This fact is also reflected in the nature of the sediment record i.e. the homogeneous organic rich clay of Gullmar Fjord versus the occurrence of discrete
intervals of laminated sediments within the Koljo¨ Fjord sequence. These observations are in accord with the geography and hydrography of Gullmar Fjord whose response to the environmental signal appears to be rather less complicated than the other more restricted fjords along the Swedish west coast. In particular the Gullmar Fjord dinoflagellate cyst spectrum can be divided into two major units as demonstrated from a visual inspection of the dinoflagellate cyst spectrum (Fig. 2), the stratigraphically constrained cluster analysis and the heterotrophic ratio (Fig. 3). These consist of an upper Unit I and a lower Unit II. However it is possible that the lower unit may also be further subdivided into three minor units. The two major units are described below: Unit I: 0.01–0.21 m; deposited between the years 1969 and 1999; this youngest unit within the sequence is characterised by a relatively high diversity of twenty-nine cyst species and over 3000 cysts per gram of sediment. In particular it contains high numbers of Protoceratium reticulatum, Spiniferites bentorii, ?Pentapharsodinium dalei, Protoperidinium avellana, Protoperidinium conicoides, Protoperidinium conicum, Protoperidinium pentagonum, Protoperidinium spp. [spiny], Islandinium cf. cesare and Polykrikos schwartzii. The particular presence of S. bentorii is perhaps indicative of a specific salinity regime possibly similar to those pertaining in the Irish Sea or indeed to seasonal localised salinity and temperature conditions (see Reid, 1974); it is not uncommon along the west coast of Sweden (Persson et al., 2000) and also in the latest Holocene sediments from Koljo¨ Fjord (Harland et al., 2004a). However it is likely that the environmental reasons for its presence are both complex and dynamic, and perhaps some seasonal overprinting has occurred as indicated by the inverse relationship between this cyst species and ?Pentapharsodinium dalei (Fig. 2), which tend to be late summer/autumn and spring/early summer species, respectively. Interestingly the other well known late summer/autumn species, Lingulodinium polyedra, is notable by its low numbers and is, therefore, not reacting to the changing environment in the same way as the other two species. The sampling is of sufficient frequency that seasonal differences will impinge upon the recovered assemblages. The log H : A ratio (Fig. 3) is within positive values throughout Unit I and reflects the high
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numbers of heterotrophic dinoflagellates present and the decline in the numbers of gonyaulacacean cysts (see also Fig. 2). Reduced frequencies of water exchanges/turnover or complete water renewal is part of a likely explanation because of the positive nature of the NAO, i.e. the increase of moisture laden westerly winds in the winter driving less saline waters towards the Swedish coast and effectively strengthening the pycnocline and acting to stabilise the water column (Nordberg et al., 2001; Bjo¨rk and Nordberg, 2003; Filipsson and Nordberg, 2004). The stability of the water column may also be reflected by the higher numbers of Spiniferites bentorii, a particular indicator of cyst production in stable and stratified late summer conditions. This dinoflagellate cyst unit is, in part, correlatable to the upper foraminiferal zone identified by Nordberg et al. (2000) and Filipsson and Nordberg (2004), indicative of declining oxygen concentrations in the bottom water and together with mostly positive NAO values, which decrease the potential for upwelling events within the Skagerrak. Parallels with the results from Koljo¨ Fjord are also evident in that its unit I, dated between 1980 and 1998, is also linked to lower bottom water salinity (Nordberg et al., 2001). Unit II: 0.22–0.60 m; deposited between the years 1915 and 1969; this older unit within the sequence is characterised by a high diversity of thirty-one species and over 4000 cysts per gram of sediment. In particular this major unit contains high proportions of Bitectatodinium tepikiense, Lingulodinium polyedrum, Spiniferites elongatus, Spiniferites mirabilis and peridinioid Protoperidinium species. The higher proportions of both B. tepikiense and L. polyedrum together with the reduction of S. bentorii are evidence of a possible salinity change and seasonal differences (see Reid, 1974). However the exact nature of these changes is difficult to establish. Rochon et al. (1999) provided histograms of the mean relative abundance of various taxa as calculated for given intervals of salinity and other physical parameters. These data suggest that B. tepikiense is most abundant at salinities (August) between 27x–36x and L. polyedrum between salinities 30x–36x, in contrast to S. bentorii, which is most abundant between salinities 34x–36x. A suggested inter-
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pretation is, therefore, that Unit II may be indicative of somewhat different salinities to Unit I but that these differences are difficult to identify and quantify. The log H : A ratio (Fig. 3), in contrast to Unit I, is within negative values and therefore indicates that there are relatively more autotrophic dinoflagellates than heterotrophic dinoflagellates, as expressed in the cyst record from the numbers of gonyaulacacean cysts. It also evident from the H : A ratio that the lowermost part of Unit II returns to positive values (Fig. 3) suggesting other changes have occurred within the environment of deposition during this time. Undoubtedly changes occurring within the sequence are many and complex involving salinity, nutrient availability and other factors. Some of these other factors will remain unknown until there is better knowledge of the ecology of dinoflagellates and their cysts. This part of the sequence in Gullmar Fjord is largely correlatable to the lower foraminiferal zone as first described by Nordberg et al. (2000) and detailed from the corresponding core by Filipsson and Nordberg (2004). It is also correlatable to mostly negative NAO values, which are indicative of a greater potential for upwelling events along the coast. In addition to the two major units the second unit may be further subdivided into the three minor units described below: a) 0.22–0.31 m; deposited between the years 1955 and 1969; characterised by low Bitectatodinium tepikiense, relatively low Lingulodinium polyedrum, relatively low Spiniferites elongatus, low Gymnodinium catenatum and relatively high Polykrikos schwartzii. b) 0.32–0.49 m; deposited between the years 1928 and 1955; characterised by high Bitectatodinium tepikiense, high Lingulodinium polyedrum, high Spiniferites elongatus, high Gymnodinium catenatum and relatively low Polykrikos schwartzii. c) 0.50–0.60 m; deposited between the years 1928 and 1915; characterised by high Bitectatodinium tepikiense, low Lingulodinium polyedrum, low Spiniferites bentorii, low S. elongatus, and high numbers of Protoperidinium conicoides, high Gymnodinium catenatum and low Polykrikos schwartzii.
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The full extent and significance of these fluctuations within the dinoflagellate cyst spectrum must await further consideration in the light of other evidence and not withstanding the lack of good and reliable autecological data.
5. Comparisons with other long term datasets As a part of this study, and to gain some insight into the changing environmental parameters through this 85-year temporal period, a series of hydrographical and historical records were consulted (see Materials and methods). The results from these are noted below and compared to the cyst record in order to gain a better understanding of the complex and dynamic system of which the dinoflagellate cyst record is only a tiny part. We believe that in so doing the relationship between the dinoflagellate cysts and hydrography, often used as a proxy for various parameters, will be available for examination within this high-resolution temporal record. 5.1. Hydrographical information In order to test the applicability of using certain cyst types as proxies for various environmental parameters, including cultural eutrophication, and taking advantage of the unique time series of hydrographical measurements available for Gullmar Fjord a series of graphs are provided herein (Figs. 3–6). These graphs variously examine the dinoflagellate cyst record against the water temperature at Alsb7ck and Borno¨; salinity at Alsb7ck and Borno¨; productivity in terms chlorophyll a and the amount of mgC m 2d 1 together with the amount of such nutrients as DIN and PO4-P; upwelling; precipitation and the air temperature at Vinga. The dinoflagellate cyst forming species commonly occurring along the west coast (Persson et al., 2000; Godhe and McQuoid, 2003) and identified as ecologically meaningful and easily identifiable include Lingulodinium polyedrum, Spiniferites bentorii, Pentapharsodinium dalei and the total number of protoperidiniacean cysts; these species were discussed in some detail in Harland et al. (2004a) and have recently been reviewed by Marret and Zonneveld (2003). In addition the total number of cysts per gram
and the heterotrophic ratio are also provided as these parameters have also been used controversially as environmental proxies (Matsuoka, 1999, 2001; Dale, 2001). The hydrographical parameters chosen to compare with the cyst record are those usually quoted in the literature as being important in the distribution of dinoflagellate cysts in bottom sediments from the marine realm. These are temperature; salinity; PO4 and DIN as a measure of nutrient availability. Plotting these various parameters in the temporal domain is less circumstantial herein than some earlier studies where the cyst records have been plotted only against an interpretation of environmental events (Dale et al., 1999). It is essential that if dinoflagellate cysts are to be used as proxies for any of the environmental parameters, including the examination of eutrophication, then the variance in their temporal record must be set against measured hydrographical variables as a test of the methodology before any confidence can be placed in their utility. The following section examines the cyst record against these various hydrographical parameters. The first of the four figures (Fig. 3), detailing the various hydrographical parameters, includes the total number of cysts per gram of sediment, the total number of protoperidiniacean cysts and the log heterotrophic ratio with the NAO index, the upwelling record and precipitation. Perusal of the diagram reveals the prominence of the change at around 1969/1970 with the increase in protoperidiniacean cysts reflected in the higher heterotrophic ratio together with the movement of the NAO into positive values and the reduction in the number of upwelling events. This correlation was noted earlier in the Results Section. A second figure (Fig. 4) examines the occurrence of the dinoflagellate cyst species, seasonally produced during the spring, against the hydrographical parameters of water temperature, salinity, upwelling frequencies and air temperature. The record of Pentapharsodinium dalei and the total protoperidiniacean cyst curve reveals increased numbers post 1970, although additionally the former does show increased numbers somewhat earlier around 1961. The spring records of the hydrographic parameters shows little differentiation except perhaps for a falling salinity trend in the Borno¨ data and a general
NAO index
log H/A ratio
Protoperidiniacean cysts/g Tot. no of cysts/g
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10000 8000 A 6000 4000 2000 0 1890 6000 4500
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3000 1500 0 1 0.5
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> 10 m > 20 m > 30 m
800 400 0 1890
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1940
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Vinga Lysekil
Fig. 3. A series of graphs detailing the total number of cysts per gram of sediment plotted against time (A); the total number of protoperidiniacean cysts per gram of sediment against time (B); the log heterotrophic ratio (C); the NAO index (D); the upwelling record (E); and the precipitation record for Vinga and Lysekil (F). The data collection and all calculations are explained in the text.
lessening of spring upwelling. Indeed the spring dinoflagellate cyst record is behaving similarly to the total cyst record and is in tune to changes within the hydrography of the fjord that has responded to the major change in the NAO i.e. a reduced number of spring upwelling events. In Fig. 5 the two dinoflagellate cysts that are produced during the late summer/autumn, i.e. Lingulodinium polyedrum and Spiniferites bentorii are plotted against the summer surface temperature and
salinity from Alsb7ck and Borno¨. There is little differentiation within the data although there is an indication that summer SST were somewhat higher between 1930 and 1970 and particularly so between 1931 and 1950; this is also seen in the averaged summer air temperatures recorded at Vinga. Using Student’s t-test the difference between the average temperatures between the two periods is statistically significant at the 95% level; hence it was 0.5 8C warmer on average and less variable. This appears to
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300
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A
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Salinity Air temp. (°C) aver. Upwelling (m) Salinity aver.
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¨ Alsback
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E
¨ Alsback
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T (°C) aver.
T (°C)
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6 3 0 35 30 25 20 15 10 28 24 20 16 10 8 6 4 2 0 9
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> 10 m > 20 m > 30 m
H
Vinga
6 3 0 1890
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1930
1940
1950
1960
1970
1980
1990
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Fig. 4. Dinoflagellate cyst and instrumental data for the spring plotted against time and including the spring dbloomerT Pentapharsodinium dalei per gram of sediment (A); the total protoperidiniacean cysts per gram of sediment (B); surface temperatures recorded at Alsb7ck (C) and Bornf (D); surface salinities recorded at Alsb7ck (E) and Bornf (F); the upwelling record (G); and the air temperature at Vinga (H). Data collection and calculations are fully explained in the text.
correspond to the raised numbers of the cysts of Lingulodinium polyedrum between the same years. Indeed the increase in numbers of Lingulodinium polyedrum starts a little earlier in 1928/1929 but
unfortunately the Borno¨ data series does not begin until 1931. The air temperature data from Vinga also reveals higher summer temperatures from about 1924 until about 1958. In addition the histogram of
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S. bentorii (cysts/g) L. polyedra (cysts/g)
Summer-Autumn 3000
1000 0 1890 300
T (°C) T (°C) aver.
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¨ Alsback
20 15 10 5 19
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E
¨ Alsback
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30 26 22
Air temp. (°C) aver. Upwelling (m)
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H
> 10 m > 20 m > 30 m
Vinga
16 13 1890
1900
1910
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Fig. 5. Dinoflagellate cyst and instrumental data for the summer–autumn plotted against time and including the late summer dbloomersT Lingulodinium polyedrum (A) and Spiniferites bentorii (B). The other graphs are as explained in the previous figure. Data collection and calculations are explained in the text.
upwelling events over the temporal record also shows an increase over these same years. Is it premature to establish a causal link between the two?
Finally Fig. 6 provides the data series for nutrients and primary productivity within the fjord at Alsb7ck and Sl7ggo¨. Unfortunately the records are limited in
PO 4-P (µM)
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A
Alsba¨ ck
1 0.5 0 1960
DIN (µM)
20
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¨ Alsback
15 10 5 0
P.P (mgC m -2 d-1)
Chl-a (µg/l)
1960 20 15
1970
1980
C
1990
Inner part
10 5 0 1985 2500 D 2000 1500 1000 500 0 1985
1990
1995
2000
¨ go¨ Slag
1990
1995
2000
Fig. 6. Instrumental data from Gullmar Fjord illustrating the phosphate concentrations in the surface waters at Alsb7ck (A); the dissolved inorganic nitrate concentrations at Alsb7ck (B); the primary production in the inner part of the fjord as expressed in the chl-a concentrations (C); and the primary production as expressed in concentrations of carbon (D). Data collection and calculations are explained in the text. The primary production series clearly shows the annual cyclicity with peaks of production generally in the spring or late summer.
their coverage, from 1960 for the nutrients and 1985 for the primary productivity, but all show little internal differentiation and only a slight increase in nutrients over the period; however there are clearly defined annual phytoplankton cycles as one would expect in these coastal fjord environments. 5.2. Local pollution history In the first half of the 20th century, that is until the mid-1960s, the innermost part of the fjord was strongly affected by industrial pollution from a sulphite pulp mill and untreated sewage outfalls from Munkedal village (Rosenberg, 1976). The pulp mill was active from 1945 to 1966, the year when it finally
closed. After 1966, when both the industrial pollution and sewage had ceased, the water quality in the innermost part of the fjord together with the benthic life recovered surprisingly quickly (Rosenberg, 1976). Beyond the mid-1970s no significant, local pollution sources were present anywhere in the fjord (Lindahl et al., 1998) and discharge from outfalls from the herring canneries and untreated sewage from the small town of Lysekil, towards the outer part of the fjord, and villages along the length of the fjord had ceased following the introduction of sewage treatment plants for both household and industrial waste. Indeed untreated sewage from water closets in Lysekil was at its worst during 1950–1975, when the population of the town was between 7000–8000. At about the same time the local canning industry was active i.e. between 1945 and 1970, with most activity in the 1950s and 1960s; finally coming to a swift decline in the 1970s. The canneries on the fjord shore produced approximately 80% of the total amount of oxygen consuming effluent and nitrogen. Interestingly the various symptoms of large scale eutrophication only began to be reported from the 1970s and 1980s at a time following the treatment of sewage, and the closing of both the Munkedal sulphite pulp mill (1966) and the herring canning industry (1970s) within the fjord.
6. Discussion The dinoflagellate cyst analysis of Core G1132Ab, taken in Gullmar Fjord, has provided one of the most detailed high-resolution records published to date. The resolution of approximately 1.5 years per sample provides a unique opportunity to examine closely the changing surface water environments within this fjord on the west coast of Sweden. It is particularly apt that this record should have been recovered from an area that boasts one of the world’s first oceanographic institutions. The dinoflagellate cyst species recovered are consistent with those recorded from modern sediments along the west coast of Sweden and documented within the literature for the area (Erdtman, 1954; Persson et al., 2000). In particular the presence of the more open marine species (see above) is entirely consistent with the open aspect of Gullmar
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Fjord in comparison to other west coast fjords particularly those that have a more restricted access to Skagerrak waters such as Koljo¨ Fjord (Harland et al., 2004a). Dinoflagellate cyst distribution patterns are largely governed by several factors, with the assumption that there has been no post mortem alteration or other taphonomic interference (see below), notably temperature (36% of the variance following the CCA of Marret and Zonneveld’s 2003 compilation of 835 samples); position within an onshore/offshore gradient (49% of the variance within their dataset); and the availability of nutrients within the surface waters including annual phosphates (33% of the variance) and annual nitrates (32% of the variance). Salinity is a well known determinant in cyst distribution patterns (Dale, 1996), but interestingly it could not be significantly related to the variance within the data of Marret and Zonneveld (2003). The dinoflagellate cyst distribution patterns generally hold true for autotrophic dinoflagellates as well as for the heterotrophs, which are ultimately reliant upon the availability and distribution of autotrophic prey species within the phytoplankton. A recently published paper on the influence of environmental factors on the distribution of cysts along the Swedish west coast (Godhe and McQuoid, 2003) has investigated the effect of 46 parameters using a variety of multivariate statistical methods. The density of the total cyst assemblages from autotrophic dinoflagellates was principally related to surface temperature and the availability of macronutrients and inversely related to the occurrence of competitors within the phytoplankton. Not surprisingly the abundance of heterotrophic dinoflagellate cyst taxa was related to their prey preference. The cyst forming dinoflagellates produce cysts as a natural part of their life cycle seemingly triggered by nutrient depletion following a phase of exponential growth; cysts typically appear in the plankton following the spring phytoplankton bloom and the late summer bloom (Pfiester, 1975; Turpin et al., 1978; Anderson and Lindquist, 1985). Recent work by Godhe et al. (2001) in a Gullmar Fjord suggests that cyst production may occur throughout the dgrowing seasonT as sexual reproduction is maintained and that temperature and light intensity has significant
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influence on cyst production. In contrast, work in Lambert’s Bay, South Africa on Zygabikodinium lenticulatum demonstrates cyst production over a short period with rapid export production through the water column (Joyce and Pitcher, 2004). Particular cyst species appear to have evolved to take advantage of either or both of these phytoplankton growth phases whereas others appear to be more opportunistic (see Harland et al., 2004b and references therein). If we assume that the regional climate has not changed markedly over the last 110 years, as can be demonstrated from the temporal series of such surface water parameters as temperature and salinity, (Figs. 3– 6), to alter significantly the cyst distribution patterns of the region then much of the temporal dinoflagellate cyst record must be attributable to changes in the availability of nutrients, trace elements and other abiotic and biotic factors on seasonal and annual timescales. However it is noteworthy that evidence is growing that recent climate warming has induced a major reorganisation of the North Atlantic pelagic ecosystem from phytoplankton to fish since the late 1980s (Beaugrand et al., 2002) and will undoubtedly impact the North Sea and contiguous waters, including their dinoflagellate flora and consequently cyst production. The availability of nutrients within the water column are variously derived from the coastal hinterland as run-off; from tidal mixing of sediments in the shallow nearshore zone especially during the winter months and around the vernal and autumnal equinoxes; and from upwelling and advection in the offshore areas. The provision of nutrients is, after latitude/temperature, the second most important determinant in phytoplankton and dinoflagellate cyst distribution patterns (see Marret and Zonneveld, 2003). In the context of the Swedish west coast the availability of nutrients to the phytoplankton derives from the surface water circulation pattern and the changing water mass types with their inherent properties of temperature, salinity and nutrient content together with various qualities such as the distribution of trace elements. Tidal energy is low and the effect of run-off is negligible in the more open aspect of Gullmar Fjord (Bjo¨rk and Nordberg, 2003). In this respect the exchange of water with the open sea, the Kattegat and Skagerrak, is all important to marine life
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in the coastal zone (Bjo¨rk and Nordberg, 2003). This water exchange is largely driven by geostrophic winds that have the effect of forcing upwelling and controlling the availability of nutrients within the system. The upwelling history, tuned from a unique longseries hydrographic dataset, suggests a declining trend between the late 1890s and 1920; an increasing frequency to 1940; and a further decline between the 1950s and 1990 (Bjo¨rk and Nordberg, 2003). These upwelling trends are mirrored, in particular, by the Lingulodinium polyedrum curve within the dinoflagellate cyst spectrum. This changing frequency in the availability of nutrients through fluctuations in summer upwelling events may be sufficient to allow such a dinoflagellate like Lingulodinium polyedrum, that thrives in stable and stratified water but can take ecological advantage of increased nutrients from depth, to increase its population size and so on encystment produce increased cyst numbers to enter the fossil record (Marret and Zonneveld, 2003; Harland et al., 2004a). However a temporal record as documented herein is also affected by taphonomic influences, which in the case of dinoflagellate cysts largely involves the availability of oxygen at the sea floor and within the sediments. It is known that certain cyst species are preferentially oxidised in these environments in the presence of oxygen (Zonneveld et al., 1997, 2001) whilst others are less susceptible. In Gullmar Fjord where the bottom sediments are sometimes subject to periods of hypoxia/anoxia, especially after 1980 (Filipsson and Nordberg, 2004), there are some increases in the numbers of protoperidiniacean cysts and the heterotrophic ratio. However the general high level of cyst recovery within the sediments, both of cysts of autotrophic and heterotrophic dinoflagellates, is suggestive that this taphonomic effect is not a problem. More recently Persson and Rosenberg (2003) have reported that dinoflagellate cyst preservation and cyst numbers occurring within bottom sediments are affected by grazing from benthic fauna. In oxygenated bottom waters grazing produced a relative increase in cyst numbers particularly in the species Lingulodinium polyedrum, Protoceratium reticulatum and Spiniferites spp. It is unlikely that this phenomenon would have much effect on the temporal record from Gullmar Fjord with its particularly high cyst recovery
(see above). Nonetheless it is important to be aware of these various taphonomic factors that could bias the fossil record of dinoflagellate cysts. The dinoflagellate cyst record documented from Core GA113-2Ab taken in the Gullmar Fjord appears to be responding to change occurring in the Skagerrak and possibly further afield in the North Sea. The coastal current running up the west coast of Sweden from the Kattegat is highly variable and responds rapidly to changes in the geostrophic wind patterns (Bjo¨rk and Nordberg, 2003). Consequential upwelling resulting from the wind patterns will control the amount of nutrients coming to the surface through advection and Ekman pumping in the offshore area and hence will have a marked effect on the dinoflagellate populations and eventually on the cyst record. The dinoflagellate cyst record detailed herein has a distinctive signature, which points to some environmental change within the marine realm at around 1969/1970. This change involves the decline in the numbers of Bitectatodinium tepikiense, and Lingulodinium polyedrum together with a concomitant increase in numbers of Spiniferites bentorii, Pentapharsodinium dalei and protoperidiniacean cysts. This environmental change is registered within those dinoflagellates producing cysts in both the spring and late summer/autumn. Examination of the various hydrographical parameters, using long sequence high resolution instrumental records, has enabled us to match this change to only two parameters. Interestingly it was not possible to identify any correspondence with temperature, salinity or indeed to nutrient content despite a possible gently rising trend in the nutrients from Alsb7ck. The only reasonable match recognised was between the dinoflagellate cyst record and the frequency of upwelling in coastal waters brought about as a consequence of the action of the NAO. As the NAO changed from a negative phase to a positive phase at around 1972/1973 the frequency of upwelling decreased. This partly corresponds with a statistically significant rise in summer temperatures at Borno¨. It is surprising that such a large and significant change in the dinoflagellate cyst populations is not reflected by a similarly large change in the hydrographic parameters but is seemly corresponding to the large scale reorganisation of the North Atlantic
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climate patterns that is characterised by the NAO. In particular the pattern of occurrence of Lingulodinium polyedrum, often now used as an indicator species for eutrophication (Sangiorgi and Donders, 2004), does not correspond to the nutrient curves or phytoplankton primary production or to the local pollution history within the fjord (see Section 5.2 (Local pollution history)). Indeed problems with large scale eutrophication within the fjord began to be reported in the 1960s interestingly at a time that the Lingulodinium polyedrum curve shows a steady decline in numbers. The simplistic use of this species as an eutrophication indicator is, therefore, not justified by these findings. Indeed our findings rather suggest that the ecology of dinoflagellates within the fjord and coastal water environment is not easily related to simple hydrographic parameters but is rather more complex and dynamic. Recent work has thrown light on the complexity of the ecology of dinoflagellates and their cysts which belies a simplistic approach to the interpretation of the fossil record. In particular our knowledge of the relationship between dinoflagellate productivity, cyst production and distribution is poor. This relationship is, however, vital if we are to link the occurrence of environmental change in surface waters to the record of dinoflagellate cysts within the sediments and more research is desperately needed, especially at a time when dinoflagellate ecology is undergoing revision. Recent research (Smayda, 2002) has pointed out certain inconsistencies in the present dinoflagellate ecological paradigm. The establishment of a stable, stratified water column is usually regarded as necessary for the high productivity of autotrophic dinoflagellates. These dinoflagellates are intolerant to shear stress caused by water mixing or turbulence and they utilise swimming strategies to occupy optimum environments; this relationship has been described using Margalef’s Mandala (see Taylor, 1987, Fig. 11A.4). However the stratification of the water column is least likely to provide nutrients and to initiate high productivity, leading to sexual reproduction and cyst production as the nutrient supply is depleted. Some dinoflagellates such as Pentapharsodinium dalei take advantage of the nutrient inoculum following the winter/spring storms whereas others, such as Lingulodinium polyedrum, favour the summer/early
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autumn. The contradiction of using the latter as an indicator of eutrophication is obvious. We have argued previously (Harland et al., 2004a) that Lingulodinium polyedrum is capable of gathering nutrients, not from an increased supply from cultural eutrophication, but rather from depth as a result of normal hydrographical processes. Smayda and Reynolds (2001, 2003) in their matrix of dinoflagellate life forms classify Lingulodinium polyedrum as a Type V (Upwelling Relaxation Taxa) involving survival strategies that include the secretion of large amounts of mucous to dampen turbulence together with high swimming speeds of 258 to 400 Ams 1 (see Smayda, 2002, Table 1). Such autecological strategies may provide Lingulodinium polyedrum with unique properties that enable it to prosper in these particular circumstances. Most recently Smayda and Reynolds (2003) have discussed the ecological strategies employed by dinoflagellates for survival. Although their discussions focus on the production of harmful algal blooms (HABs) some factors are pertinent to the interpretation of the fossil record. In order to survive dinoflagellates as a group must be able to tolerate high physical disturbance, light stress and nutrient limitations and not only to enjoy optimal conditions but also to cope with less than optimal environments. Adaptive strategies have arisen as a coping mechanism and can be recognised within a number of species associations including C-strategists (competitors), S-strategists (stress tolerant species) and R-strategists (ruderal or disturbance tolerant species). Originally applied to freshwater species (Reynolds, 1988) this concept can be applied to the marine realm (Smayda and Reynolds, 2003) and to the cyst forming dinoflagellates. Indeed many of the cyst forming dinoflagellates are well known in neritic environments and appear to be R-strategists in order to overcome the shear stress associated with turbulence and water mixing often prevalent in these environments. Not withstanding that much of this work stems from the study of HABs the ecology of dinoflagellates is organised around associations of species reacting to abiotic factors of irradiance, nutrients and turbulence with species selected to fulfil one of the strategies described above. This relatively simple plan (the 3-3 plan of Smayda and Reynolds, 2003) will encompass the production of cysts as a part of the ecological expedient to survive neritic environments.
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In the present study the dinoflagellate cyst record is an amalgam of this ecological paradigm as applied to all the species recorded and cannot be regarded as a simple set of curves reacting to simple changes in the environment. We have focused upon Lingulodinium polyedrum as it has and is being used as an indicator of eutrophication and Pentapharsodinium dalei, a cyst most often used to indicate cold climate conditions. Our work reveals patterns of change within the cyst record reflecting changes in the NAO rather than with any simple abiotic parameter. For the former this may be the result of increased nutrient availability from depth as a result of increased frequencies of upwelling or it might showcase the R-tolerance of the species and hence be able to thrive in waters subjected to increased overturn, upwelling as a result of a particular NAO regime; it is also likely to be a K strategist. It is suspected that the former is also Rtolerant but also an r strategist more amenable to the unpredictable and instability of the spring environment closely following on from the equinoxal storms. It is clearly a complex situation and one that can be argued from several different viewpoints. This study demonstrates the complexity and seeks to avoid a simplistic abiotic interpretation but rather looks to rather larger scale changes within the hydrographic regime reacting to change within the climate patterns within the North Atlantic. To explore some of these ideas further and to look in more detail at other dinoflagellate cysts within our records is outside the scope of this contribution but will ultimately provide a clearer interpretation of the changing marine environment at the annual to decadal scale, a temporal scale so important for predicting our futures.
7. Conclusions This detailed study of the dinoflagellate cyst record of a high resolution sediment record from Gullmar Fjord on the west coast of Sweden has led to some surprises. Contrary to received wisdom the cyst record shows little correlation with the putative ongoing eutrophication in the fjord, and along the west coast of Sweden. Indeed the record of Lingulodinium polyedrum, a suggested index species for eutrophication does not show an ongoing increase in numbers but rather shows a marked decrease since 1970. Its presence within the dinofla-
gellate cyst record is most marked from about 1929 until 1970 having little correlation with the many abiotic instrumental data available from this well studied area and also the known local pollution history. We, therefore, cannot confirm an ongoing eutrophication problem for Gullmar Fjord using the dinoflagellate cyst record nor can we endorse the use of Lingulodinium polyedrum as an eutrophication indicator. In contrast there is a clear change in the dinoflagellate cyst populations at around 1970, as detailed in both spring and late summer cyst producers, which is clearly indicative of a major change in the environment. The only change noted in our study is that accompanying the changeover from a largely negative to positive NAO at about the same time by a decrease in the frequency of upwelling events in the offshore Skagerrak area. The response of the dinoflagellate populations to this change is not easily explained as it is likely to be complex and dynamic. Some attempt has been made to examine these results in the light of a recently published ecological paradigm but a definitive conclusion is not possible at the moment. However we advise against a simplistic interpretation and trust that further work on the ecology of the cyst-forming dinoflagellates might clarify the situation further.
8. Systematic section This section lists the dinoflagellate cysts recovered in Core GA113-2Ab, Gullmar Fjord, Sweden. Taxonomic references can be found in Fensome et al. (1993) for the most part but otherwise are provided herein. Illustrations of many of the relevant dinoflagellate cyst taxa recovered in our study can be found in Rochon et al. (1999) and Harland et al. (2004b), from comparable material in the general North Atlantic area and along the west coast of Sweden. It is beyond the scope of this contribution to provide a fully comprehensive and detailed taxonomic study but the material is available at the University of Go¨teborg. Division DINOFLAGELLATA (Bqtschli, 1885) Fensome et al., 1993. Class DINOPHYCEAE Pascher, 1914. Order GONYAULACALES Taylor, 1980. Family GONYAULACACEAE Lindemann, 1928.
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Genus Ataxiodinium Reid, 1974. Ataxiodinium choane Reid, 1974. Genus Bitectatodinium Wilson, 1973. Bitectatodinium tepikiense Wilson, 1973. Genus Lingulodinium Wall, 1967 emend. Dodge, 1989. Lingulodinium polyedrum (Stein, 1883) Dodge, 1989. Genus Nematosphaeropsis Deflandre et Cookson, 1955 emend. Wrenn, 1988. Nematosphaeropsis labyrinthus (Ostenfeld, 1903) Reid, 1974. Genus Protoceratium Bergh, 1882. Protoceratium reticulatum (Clapare`de et Lachmann, 1859) Bqtschli, 1885. Genus Spiniferites Mantell, 1850 emend. Sarjeant, 1970. Spiniferites bentorii (Rossignol, 1964) Wall et Dale, 1970. Spiniferites delicatus Reid, 1974. Spiniferites elongatus Reid, 1974. Spiniferites lazus Reid, 1974 Spiniferites mirabilis (Rossignol, 1964) Sarjeant, 1970 Spiniferites ramosus (Ehrenberg, 1838) Mantell, 1854. Spiniferites spp. indet. Order PERIDINIALES Haeckel, 1894. Family PERIDINIACEAE Ehrenberg, 1831. Genus Pentapharsodinium Indelicato et Loeblich III, 1986. ?Pentapharsodinium dalei Indelicato et Loeblich III, 1986. Family PROTOPERIDINIACEAE Bujak et Davies, 1998. Genus Islandinium Head et al., 2001. Islandinium cf. cesare (de Vernal et al., 1989 ex de Vernal in Rochon et al., 1999) Head et al., 2001. Genus Lejeunecysta Artzner et Do¨rho¨fer, 1978 emend. Lentin et Williams, 1976. Lejeunecysta marieae (Harland in Harland et al., 1991) Lentin et Williams, 1993. Lejeunecysta oliva (Reid, 1977) Turon et Londeix, 1988. Genus Protoperidinium Bergh, 1881. Protoperidinium avellana (Meunier, 1919) Balech, 1974.
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Protoperidinium claudicans (Paulsen, 1907) Balech, 1974. Protoperidinium compressum (Abe´, 1927) Balech, 1974. Protoperidinium conicoides (Paulsen, 1905) Balech, 1974. Protoperidinium conicum (Gran, 1900) Balech, 1974. Protoperidinium divaricatum (Meunier, 1919) Parke et Dodge, 1976. Protoperidinium leonis (Pavillard, 1916) Balech, 1974. Protoperidinium oblongum (Aurivillius, 1898) Balech, 1974. Protoperidinium pentagonum (Gran, 1902) Balech, 1974. Protoperidinium punctulatum (Paulsen, 1907) Balech, 1974. Protoperidinium subinerme (Paulsen, 1904) Loeblich, 1969. Protoperidinium spp. indet. [peridinioid]. Protoperidinium spp. indet. [round, brown]. Protoperidinium spp. indet. [short spines]. Order GYMNODINIALES Apstein 1909. Family POLYKRIKACEAE Kofoid et Swezy 1921. Genus Gymnodinium von Stein, 1878. Gymnodinium catenatum Graham 1943. Genus Polykrikos Bu¨tschli, 1873. Polykrikos schwartzii Bqtschli 1873. Family UNCERTAIN. Cyst nov. [sparse, spiny].
Acknowledgements The authors would like to thank the crew of the RV Arne Tiselius and RV Skagerak for their assistance in collecting the cores and Mr Steve Ellin and Ahwad B Ibrahim for their technical expertise in processing the samples in the laboratories of the Palynology Research Facility, University of Sheffield. The study was financed by the Swedish Natural Science Research Council (NFR, grants no. G-AA/GU 09874-307 and G-AA/GU 09874-309, K. Nordberg), the Futura Foundation, the Oscar and Lili Lamm Foundation, the Carl Trygger Foundation, the
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Rochon A, de Vernal A, Turon J-L, Matthiessen J, Head MJ. Distribution of recent dinoflagellate cysts in surface sediments from the North Atlantic Ocean and adjacent seas in relation to sea-surface parameters. Contrib Ser, Am Assoc Stratigr Palynol 1999;35:1 – 146. Rosenberg R. Negative oxygen trends in Swedish coastal bottom waters. Mar Pollut Bull 1990;16:335 – 9. Rosenberg R, Cato I, Fo¨rlin L, Grip K, Rodhe J. Marine environment quality assessment of the Skagerrak–Kattegat. J Sea Res 1996;35:1 – 8. Rydberg L. Hydrographic observations in the Gullmar Fjord during April 1973. Report, vol. 10. Sweden7 Department of Oceanography, University of Go¨teborg; 1975. p. 1 – 14. Sangiorgi F, Donders TH. Reconstructing 150 years of eutrophication in the north-western Adriatic Sea (Italy) using dinoflagellate cysts, pollen and spores. Estuar Coast Shelf Sci 2004;60:69 – 79. Smayda TJ. Turbulance, watermass stratification and harmful algal blooms: an alternative view and frontal zones as bpelagic seed banksQ. Harmful Algae 2002;1:95 – 112. Smayda TJ, Reynolds CS. Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. J Plankton Res 2001;23:447 – 61. Smayda TJ, Reynolds CS. Strategies of marine dinoflagellate survival and some rules of assembly. J Sea Res 2003;49: 95 – 106. Svansson A. Hydrography of the Gullmar fjord. Med Havsfiskelab Lysekil. Inst Hydrogr Res Go¨teb, Sweden, vol. 23; 1984. p. 1 – 21. Taylor FJR. The biology of dinoflagellates. Bot Monogr, vol. 21. Oxford7 Blackwell Scientific Publications; 1987. p. 1 – 785. Turpin DH, Dobell PER, Taylor FJR. Sexuality and cyst formation in Pacific strains of the toxic dinoflagellate Gonyaulax tamarensis. J Phycol 1978;14:235 – 8. Wall D, Dale B. Modern dinoflagellate cysts and evolution of the Peridiniales. Micropaleontology 1968;14:265 – 304. Wood GD, Gabriel AM, Lawson JC. Palynological techniques— processing and microscopy. In: Jansonius J, McGregor DC, editors. Palynology: Principles and Applications, vol. 1. Salt Lake City7 American Association of Stratigraphic Palynologists Foundation; 1996. p. 29 – 50. Zonneveld KAF, Versteegh GJM, de Lange GJ. Preservation of organic-walled dinoflagellate cysts in different oxygen regimes: a 10,000 year natural experiment. Mar Micropaleontol 1997; 29:393 – 405. Zonneveld KAF, Versteegh GJM, de Lange GJ. Palaeoproductivity and post-depositional aerobic organic matter decay reflected by dinoflagellate cyst assemblages of the Eastern Mediterranean S1 sapropel. Mar Geol 2001;172:181 – 95.
Dinof lagellate cysts and hydrographical change in Gullmar Fjord, west coast of Sweden Rex Harlanda,T, Kjell Nordbergb, Helena L. Filipssonc b
a DinoData Services, 50 Long Acre, Bingham, Nottingham NG13 8AH, UK Department of Oceanography, Earth Sciences Centre, Go¨teborg University, P.O. Box 460, S-40530, Go¨teborg, Sweden c University of Bremen, FB 5 Geosciences, P.O. Box 330 440, DE-28334 Bremen, Germany
Received 20 September 2004; accepted 18 February 2005 Available online 9 June 2005
Abstract This high-resolution study of the latest Holocene dinoflagellate cyst record from Gullmar Fjord, on the west coast of Sweden, provides evidence for the recognition of two major dinoflagellate communities within the fjord over the last 85 years. These communities may have their origins with the history of cultural eutrophication within the region, but are more likely to be associated with the wider phenomenon of the North Atlantic Oscillation and/or the complex hydrographical response of the fjord to various changing climatic environments between 1915 and 1999. The changing dinoflagellate cyst populations are compared in detail with the many hydrographical parameters available from this well studied fjord with its long instrumental records. Indeed the dinoflagellate cysts fail to demonstrate a convincing ongoing eutrophication record for the fjord but do show a major change in the cyst assemblages at about 1969/1970 at a time when the NAO was changing from a negative phase to the present-day positive phase. Gullmar Fjord is important in the history of dinoflagellate cyst studies, being the site of the 1954 study by Erdtman in which viable cysts, produced within the phytoplankton, were first documented within the water column. D 2005 Elsevier B.V. All rights reserved. Keywords: Dinoflagellate cysts; Eutrophication; North Atlantic oscillation; Coastal upwelling; Gullmar Fjord; West coast of Sweden
1. Introduction Marine offshore cultural eutrophication in Scandinavian waters is considered to be a major pollution problem, and has been the focus of research among a large number of marine scientists, for about twenty
T Corresponding author. Tel.: +44 1949 875287. E-mail address: [email protected] (R. Harland). 0048-9697/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2005.02.030
years (e.g. Baden et al., 1990; Diaz and Rosenberg, 1995; Nixon, 1995 and references therein). The consensus is that there has been an increase in the amount of sewage and agricultural fertilisers in the North Sea, including the Skagerrak, Kattegat and Baltic Sea, since the 1960s (Aure et al., 1996; Rosenberg et al., 1996). This has led in some locations, especially those additionally subjected to local drainage outlets and sewage outfalls, to enhanced primary production, altered algal composi-
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tion, decreased secci depth, increased accumulation of oxygen consuming organic material on the sea floor, oxygen deficiency in bottom water and subsequent benthic mortality.
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Gullmar Fjord is one of a series of sill fjords along the west coast of Sweden, north of Go¨teborg, in which this problem has been manifest. The fjord (Fig. 1) is some 30 km long and 2 km wide and
Fig. 1. Location map of Gullmar Fjord showing the site of core G113, the source of local pollution from Lysekil and Munkedal and the locations of the stations from which the instrumental data have been sourced. Vinga Island is located approximately 10 km west of Gfteborg (Gbg).
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has a maximum depth of 119 m. It is orientated in a NE/SW direction and opens into the Skagerrak across a sill at 42 m depth. The fjord is subjected to strong stratification with pycnoclines occurring at depths of between 15 and 20 m (Svansson, 1984), separating upper low salinity waters (24–27 psu) from more saline waters (32–33 psu), and between 50 and 60 m separating those waters from the highly saline waters (34–35 psu) in the deeper parts of the fjord (Lindahl et al., 1998; Arneborg, 2004). This stratification arises from the presence of low salinity Baltic water at the surface in the Skagerrak (Gustafsson, 1999; Bjo¨rk and Nordberg, 2003) and higher salinity North Sea and North Atlantic water at depth. The stability of the water stratification is variously enhanced by the influx of freshwater from ¨ rekils7lven at the head of the fjord, the the river O presence of sea-ice during cold winters and a small, semi-diurnal tidal range (0.15–0.30 m). The residence time of the low saline surface water is about 16–26 days and that down to the sill depth is about 40 days (Arneborg, 2004). Instrumental records demonstrate that the residence time of the surface waters has not changed between 1954 and 1986 and no decreasing or increasing trends have been recognised (Arneborg, 2004). The deeper more saline waters are relatively stagnant and are usually only exchanged during the winter or spring months when northerly to easterly winds induce upwelling due to Ekman pumping in the coastal waters (Rydberg, 1975). The deepest parts of the fjord, below 80 m, are occasionally subjected to hypoxic conditions during the autumn and winter as oxygen levels inevitably fall progressively throughout the year. However, since the late 1960s and early mid 1970s, it is accepted by the scientific community that Gullmar Fjord has not been subjected to any major source of water pollution from either sewage or industry (see later discussion). Before that, the inner part of the fjord received large amounts of oxygen-consuming substances from a paper mill, a sulphite mill (founded in the 1870s) and other anthropogenic activities (Rosenberg, 1990). In Lysekil, in the outer part of the fjord, untreated sewage and outlets from herring canneries ceased during the early 1970s. Nowadays it is acknowledged that there are no major sources of water
pollution from either sewage or industry within the environs of the fjord (Lindahl et al., 1998). In spite of this, and the closure of factories and the establishment of ambitious sewage treatment plants, little improvement has been noted in the quality of water from the fjord or indeed anywhere along the Swedish west coast. Therefore despite the lack of significant local sources of pollutants within the fjords, human induced eutrophication is still considered as ongoing and worsening (Rosenberg, 1990; Lindahl et al., 1998). Lately, however, this conventional wisdom has been challenged by research indicating a significant connection between the hydrography of the fjords on the Swedish west coast, with weather conditions/ climate on a decadal time scale, and larger scale marine pollution. In particular it has been demonstrated that variations in climate, in combination with the fjord morphology, has influenced the marine environment in respect to the frequency of water renewals in the fjords with the possible consequential establishment of stagnant bottom water, oxygen deficiency and benthic mortality (Nordberg et al., 2000, 2001). During the last 20 years or so the winters have been mild, humid and characterised by predominantly westerly winds (Bjo¨rk and Nordberg, 2003). This pattern has had a significant negative influence on both coastal and fjord environments with a marked decrease of renewal events. A major problem is, however, that the influence from human impact and the changes in the climate have acted almost simultaneously and thereby largely prevented the possibility of separating artificial and cultural effects from natural causes. Indeed recent research has suggested that there is a possible causal relationship between variations in the North Atlantic Oscillation (NAO) and the marine environment within Gullmar Fjord (Lindahl et al., 1998, 2003; Nordberg et al., 2000). In particular an indirect link between the NAO, the supply of nutrients and primary production has been suggested (Lindahl et al., 1998). This relationship has also been explored in an adjacent fjord, Koljo¨ Fjord, which is more restricted in its access to the Skagerrak than Gullmar Fjord (Harland et al., 2004a,b). Both fjords appear to react to the activity of the NAO in somewhat different ways
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seemingly as a direct consequence of their unique hydrography. The analysis of sediments deposited in Gullmar Fjord, and their contained foraminiferal faunas, have detailed a striking faunal change during the mid 1970s from a normal Skagerrak-Kattegat fauna to an opportunistic low oxygen fauna (Nordberg et al., 2000; Filipsson and Nordberg, 2004). Recent revisions to the dating of this event favour the year of 1979, which may relate to a widespread low oxygen event occurring in 1979/1980 (Filipsson and Nordberg, 2004). This appears to follow the change from negative winter NAO to positive winter NAO and the establishment of mild, humid winters and prevailing westerly winds. These westerly winds move low saline Baltic waters towards the coast (Gustafsson and Stigebrandt, 1996; Gustafsson, 1999), which lessens the frequency of upwelling events and the consequential exchange of bottom waters in the fjord so enhancing the depletion of oxygen (Nordberg et al., 2000; Bjo¨rk and Nordberg, 2003).
2. Historical note Gullmar Fjord is one of the most studied marine areas in the world with the first hydrographical measurements being taken as early as 1869. Indeed the Kristineberg Marine Research Station, one of the world’s oldest marine research stations, was founded in 1877 by the Royal Swedish Academy of Sciences at Fiskeb7ckskil on the shores of the fjord (Fig. 1). In 1954 Erdtman published one of the first studies, if not the first, on the occurrence of living dinoflagellate cysts, produced by the local phytoplankton, settling through the water column of the fjord over the years 1947 to 1949. The material was collected in bottomless corked flasks, fixed inverted 15 m below mean sea level and some 22 m from the shore. The flasks were changed monthly and the sediment analysed following treatment with hydrogen fluoride and acetolysis. The dinoflagellate cysts recovered were identified by Professor Trygve Braarud and figured in the consequent publication. The cysts include Protoceratium reticulatum (?Islandinium minutum) Fig. 1A; cf. Peridinium triquetrum (Protoceratium reticulatum) Fig. 1B; dnot a dinoflagellate cystT (?Spini-
207
ferites bentorii) Fig. 1C; dprobably a dinoflagellate cystT (?Spiniferites sp. indet.) Fig. 1D; dpart of a dinoflagellate cystT (?Incertae sedis) Fig. 2A; cf. Goniaulax polyedra (Lingulodinium polyedrum) Fig. 2B; Goniaulax polyedra (Lingulodinium polyedrum) Fig. 3A; and dprobably a dinoflagellate cystT (Protoceratium reticulatum) Fig. 4. The identifications provided in parentheses are our interpretations of the species illustrated by Erdtman (1954) with their modern epithets. It is interesting to note that in this early pioneering work the cysts collected were recognised as being viable and, therefore, not reworked and that they might prove useful in marine stratigraphy. Erdtman (1954, p. 110) asked bWill it be possible to use, to some extent at least, hystrichosphaerids and hystrichosphaeridoid organisms in the same way as pollen grains and spores in peats and lacustrine sediments? If this can be done, marine sediments poor in pollen grains or lacking them altogether, would, nevertheless, be accessible to micropalaeontological investigations similar to pollen statistics.Q In the context of our research, detailed herein, it is relevant to reiterate some of Erdtman (1954) original findings. In particular he noted that the dsporesT of Goniaulax polyedra (Lingulodinium polyedrum) were common in some samples especially in September and the first week in October when they were sixty-six times more frequent than the recovered pollen grains. In addition the palynological assemblages collected over this autumnal period were twice as large as those collected during the spring pollen maximum in May. Recent opportunistic research on the seasonal production of dinoflagellate cysts, as trapped within the flocculent layer (Harland et al., 2004b), from Koljo¨ Fjord is consistent with Erdtman’s earlier findings and confirms and identifies Lingulodinium polyedrum as a species that produces cysts towards the end of the summer and into the early autumn as also noted previously by Dale (1976) and Lewis and Hallett (1997). The relationship between planktonic dinoflagellates and cyst production in Gullmar Fjord has been explored rather more recently using sediment traps deployed for short three-day periods from the end of May to mid-June 1998 (Godhe et al., 2001). The seasonality of cyst production was demonstrated and the commonest species in the traps and plankton were
208
Core GA113–2Ab Dinoflagellate Cyst Analysis Analyst: R Harland
Peridiniacean and Protoperidin’ cysts
Gymnodinialean cysts
1985 -
0.10
1978 -
0.15
1971 -
0.20
1964 -
0.25
1957 1950 -
Depth (m)
0.05
YS i
LL
tzi
GE
ar
LA
hw
OF
sc
LD
IN
os
TA TO
Po
lyk
rik
din no m Gy
AT
tu na te ca ium
niu idi er op ot Pr
EC
m
et ind p. sp m
m niu idi er op ot Pr
TS
B] .[R
ud um nic co
nic co Pr
?P
ot
en
op
ta
er
ph
idi
ar
niu
so
m
din
ng elo es rit fe ini Sp
/n
es oid
lei ium
us at
ii or nt be es rit fe ini Sp
Pr
da
tu ula tic re ium at er oc ot
lod gu Lin
0.00 1992 -
Bi
te
cta
to
ini
din
um
ium
po
te
lye
pik
dr
a
ien
m
se
um
Gonyaulacacean cysts
Zone
CONISS
Unit I
Unit IIa
0.30 0.35
1942 -
0.40
1935 -
0.45
1928 -
0.50
1921 -
0.55
1914 -
0.60
Unit IIb
Unit IIc
100 200 300 400 0.65
1000 2000 3000
1000 2000 3000
100
200
300
50
100
150
100
200
300
20
40
60
80
100
100 200 300 400 500
1000 200030004000 5000
100 200 300 400
100 200 300 400
200040006000800010000
20000 40000 60000 80000 Total sum of squares
Fig. 2. Dinoflagellate cyst spectrum of selected species from Core GA113-2Ab, constructed using the cyst per gram data. The CONISS cluster analysis together with the visual inspection allows the core to be subdivided into the informal units as shown and described in the text. The 210Pb dating is indicated on the left of the figure.
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gullmar Fjord
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Pentapharsodinium dalei, related Scrippsiella spp. and Protoceratium reticulatum. Gonyaulax spinifera was absent from the plankton although some cysts were recovered from the sediment traps; Lingulodinium polyedrum was rarely observed in the plankton but was absent in the traps. Pentapharsodinium dalei is known as a spring blooming species in contrast to Lingulodinium polyedrum, which is well documented as favouring the late summer/autumn (see above). Godhe et al. (2001) found no linear relationship between cyst forming species in the plankton and the number of cysts in the traps. They also demonstrated, using multiple regression analysis, correlation with SST, ambient light radiation, and the halocline depth in contrast to the nutrient concentrations that appeared to correlate only poorly. It was noted that the dinoflagellates were undergoing sexual reproduction throughout the period of study and that temperature and light intensity appear to be of some importance in cyst formation. It is with this particular background that this new analysis of the dinoflagellate cysts from Gullmar Fjord was initiated as part of a larger study aimed at understanding the relationship between climate, hydrography and oxygen deficiency in bottom water from fjords along the west coast of Sweden. An analysis of the highresolution temporal record of the dinoflagellate cysts occurring in the latest Holocene sediments was, therefore, carried out to provide a proxy record for environmental change within the surface waters of the fjord. It was anticipated that comparison with results available from the restricted Koljo¨ Fjord would prove to be particularly useful to our understanding of the response of the west coast of Sweden to various changes both natural and cultural. In particular a primary aim of the study was to attempt to disentangle the effects of natural climatic fluctuations from cultural disturbances such as eutrophication and marine pollution. The analysis of dinoflagellate cysts is increasingly being used to document eutrophication and various aspects of marine pollution in coastal waters (Dale, 1996, 2001; Matsuoka, 1999, 2001; Pospelova et al., 2002, 2004; Sangiorgi and Donders, 2004) with much of this discussion published within the pages of The Science of the Total Environment.
209
3. Materials and methods 3.1. Sampling and processing The sediment core site G113, situated at Lat: 588 18V95 N and Long: 118 32V36 E (Fig. 1) was sampled by several cores taken in June 1999 by the r/v Skagerak using a Gemini Corer. This method of core collection provides a virtually undisturbed sediment/water interface and a core some 80 mm in diameter and 610 mm in length. After collection the cores were X-rayed on board ship with an Andrex BV (155 140 Kv/5mA) portable machine before further investigation. In the laboratory the cores were sliced and analysed for their organic carbon content using a Carlo Erba NA 1500 instrument. Radiometric dating using the 210Pb methodology and the constant rate of supply (CRS) model of Appleby and Oldfield (1978) was carried out at the Department of Radiation Physics, University of Lund, Sweden on one of the cores, GA113-1A, (see Nordberg et al. (2001) and Filipsson and Nordberg (2004) for further details and the age depth profile). A correlation with the core analysed herein, GA113-2Ab, was effected using foraminiferal marker levels and in particular the marked increase in the proportions of the opportunistic foraminifera Stainforthia fusiformis (Williamson). The sediment accumulation rate was calculated at 0.7 cm/year and the dating is indicated on the dinoflagellate cyst spectrum (Fig. 2). A suite of sixty samples was taken from the recovered core GA113-2Ab, (the original core GA113-2A was split so that one half, GA1132Aa, was analysed for foraminifera whereas the second, GA113-2Ab, was analysed for both diatoms (see McQuoid and Nordberg, 2003) and dinoflagellate cysts), at a sample interval of 1 cm and, therefore, encompassing some 60 cm of sediment. The sediment is homogenous, organicrich clay (Nordberg et al., 2000) and it is estimated from the 210Pb radiometric dating study on core GA113-1A that the suite of samples represents a time interval from 1915 until 1999. All the samples were processed to extract the dinoflagellate cysts using the normal palynological processing techniques as described by Wood et al. (1996). In
210
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
particular the samples were treated consistently throughout to maintain the integrity of the dataset. The samples were not subjected to any oxidising reagents to prevent the differential loss of protoperidiniacean cysts (Dale, 1976; Zonneveld et al., 1997) but were subjected to prolonged washing and filtering together with the use of ultrasound, up to 2 min, to free the dinoflagellate cysts from the amorphous organic material (AOM) that is always present in these nearshore fjord samples. The resulting palynological residues were stained with Safranin and dispersed onto microscopical coverslips using Elvacite and bonded to slides using Petrapoxy 154 resin, which has a refractive index of 1.54. In addition the samples were treated quantitatively so that the numbers of cysts per gram of sediment could be calculated. The original dry weight of sediment was noted; usually 5 g in this instance, and aliquot subsamples of the organic residues were taken for mounting and counting (Harland, 1989). Samples were counted on a single slide, representing either 1 g of original sediment or a fraction thereof, with a 40 objective using a Zeiss Axiolab microscope. The derived data are detailed in Tables 1 and 2 and include the raw counts and the calculated number of cysts per gram of sediment, respectively. TILIA/TILIAGRAPH software has been used to construct a dinoflagellate cyst spectrum and Fig. 2 illustrates the spectrum based upon certain selected species. A full taxonomic listing of the recovered cysts can be found in the short systematic section to this contribution. 3.2. Data treatment 3.2.1. Dinoflagellate cysts Stratigraphically constrained incremental sum of squares cluster analysis using CONISS (Grimm, 1987) as part of the software package has also been employed in the analysis of the dinoflagellate cyst assemblages to differentiate the various assemblages through the core and to assist in the visual interpretation of the diagram, and a heterotrophic ratio was calculated from the numbers of dinoflagellate cysts present within the samples (Powell et al., 1990; Dale, 1996). This heterotrophic ratio is simply the numbers of cysts from heterotrophic dinoflagellates divided by
those identified as derived from autotrophic dinoflagellates and expressed as a log value (Fig. 3). The first use of such a ratio to express differences within the cyst assemblages was published by Harland (1973) who recognised the different apparent ecological requirements of gonyaulacacean and peridiniacean cysts from their distributions in modern sediments as known at the time (Wall and Dale, 1968); this was later expressed and explained as fundamental differences in trophic behaviour (Harland, 1988). The trophic assignment of the various species is provided in the taxonomic listing. High values of the ratio are indicative of the greater presence of the cysts of heterotrophic dinoflagellates. Relative increases of heterotrophic dinoflagellates, as evidenced by their cyst production, have been used to indicate the increased presence of their prey species. This has been assumed to indicate the probable enhancement of nutrients as the phenomenon has been linked to areas of upwelling (see Powell et al., 1990, etc.). Heterotrophic dinoflagellates often prey upon diatoms as a first choice and, therefore, as diatom numbers rise, in response to increased nutrient supply, the heterotrophic dinoflagellate populations follow; the fundamental assumption is that this effect produces a higher cyst yield. However apparent increases in the proportions of heterotrophic dinoflagellates can also be caused by a decrease in the proportions of autotrophic dinoflagellate cysts; it is often difficult, if not almost impossible, to disentangle this phenomenon (see discussion). Unfortunately for the moment there is no research available that securely links these phenomena into a coherent picture much less providing a model that can be used for palaeoecological interpretations. It is, therefore, advisable to treat the use of the heterotrophic ratio as a guide only and with a significant amount of caution until a model is available based with confidence upon modern data. 3.2.2. Hydrographic and atmospheric data In order to compare the data from different instrumental records with the dinoflagellate cyst record the data sets had to be treated differently, especially with respect to averaging over time, as the sampling density between them varied. All the surface water data was, however, depth averaged between 0–10 m. We present this yearly hydro-
Table 1 Dinoflagellate cyst analysis as raw counts Gullmar Fjord, Sweden Core GA113-2Ab Raw counts
RH414 RH415 RH416 RH417 RH418 RH419 RH420 RH421 RH422 RH423 RH424 RH425 RH426 RH427 RH428 RH429 RH430 RH431 RH432 RH433 0.01 m 0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09
0.1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19
0.2
0 4 2 0 64 7 0 0 0 0 0 9
0 2 6 0 64 0 0 3 0 0 0 9
0 3 12 0 41 0 0 0 0 0 0 3
0 5 0 0 49 4 0 1 0 0 0 9
0 0 0 0 62 3 0 1 0 0 0 8
1 0 4 0 53 3 0 0 0 0 0 10
0 0 6 0 33 1 0 1 0 0 1 5
0 0 0 0 36 3 0 5 0 0 1 11
0 0 5 0 75 5 1 0 0 0 0 14
0 2 0 0 103 6 0 1 0 0 0 9
1 0 1 0 55 5 0 2 0 0 0 10
0 0 2 0 43 9 0 2 0 0 0 10
0 0 7 0 57 3 0 1 0 0 2 9
0 1 1 0 41 10 0 0 0 0 0 18
2 0 0 0 33 15 0 1 0 0 1 13
0 1 13 0 60 13 1 2 0 0 2 19
0 1 11 0 41 7 0 2 0 1 0 17
0 3 21 0 31 10 2 3 0 0 0 13
0 2 11 0 59 2 0 0 0 0 0 7
2
0
4
5
14
4
6
12
11
2
5
0
2
0
0
3
3
3
2
2 0 0 1 0 3 9 0 0 3 3 3 0 0 1 132 0
3 0 0 2 0 0 5 0 0 0 0 0 3 0 0 112 1
9 0 0 0 0 6 11 0 0 1 3 2 0 1 0 131 3
41 0 1 1 3 3 15 0 0 1 2 0 1 0 0 251 6
28 0 1 0 0 3 23 0 1 0 6 1 0 0 0 251 4
13 0 0 0 1 5 11 0 0 2 4 0 0 0 0 156 4
7 0 1 0 0 0 6 0 0 1 3 0 0 0 0 84 1
6 0 0 0 0 4 15 0 0 0 3 1 0 0 0 96 2
3 0 0 0 0 6 10 1 0 0 2 1 0 1 0 119 4
1 0 1 0 0 2 9 0 0 2 2 0 0 0 0 128 6
9 0 0 0 1 13 9 0 1 1 2 0 1 0 0 174 1
1 0 0 0 0 1 7 0 0 0 5 1 2 0 0 102 3
7 0 0 0 0 5 25 0 0 3 2 2 1 0 2 157 4
2 0 3 0 0 1 14 0 0 3 3 0 0 0 0 164 6
3 0 4 0 2 0 19 0 1 1 7 1 3 0 0 186 7
3 0 3 0 0 2 16 0 1 1 4 0 1 2 0 136 3
4 0 0 0 3 2 10 0 0 0 0 0 1 0 0 99 4
4 0 0 0 0 1 6 0 1 1 0 0 0 0 0 66 0
0 0 0 0 0 0 9 0 0 3 0 0 0 0 0 84 3
0 5 8 257
0 2 3 221
0 12 6 248
0 21 8 427
0 4 9 419
0 2 8 281
0 5 4 165
0 11 13 219
0 10 7 275
0 10 9 293
0 11 14 316
0 9 2 199
0 9 8 306
0 11 19 297
0 9 17 328
0 5 10 301
0 4 15 225
0 0 23 188
0 5 5 192
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane 0 Bitectatodinium tepikiense 0 Lingulodinium polyedrum 1 Nematosphaeropsis labyrinthus 0 Protoceratium reticulatum 8 Spiniferites bentorii 4 Spiniferites delicatus 0 Spiniferites elongatus 0 Spiniferites lazus 0 Spiniferites mirabilis 0 Spiniferites ramosus 0 Spiniferites spp. indet. 9 Peridiniacean cysts ?Pentapharsodinium dalei 0 Protoperidiniacean cysts Islandinium cf. cesare 1 Lejeunecysta marieae 0 Lejeunecysta oliva 0 Protoperidinium avellana 0 Protoperidinium claudicans 0 Protoperidinium conicoides 5 Protoperidinium conicum/nudum 12 Protoperidinium compressum 0 Protoperidinium divaricatum 0 Protoperidinium leonis 1 Protoperidinium oblongum 1 Protoperidinium pentagonum 0 Protoperidinium punctulatum 0 Protoperidinium subinerme 0 Protoperidinium spp. indet. [P] 0 Protoperidinium spp. indet. [RB] 104 Protoperidinium sp. nov. 0 Gymnodinialean cysts Cyst nov. [sparse spiny] 0 Gymnodinium catenatum 6 Polykrikos schwartzii 5 n 157
(continued on next page)
211
212
Table 1 (continued) Gullmar Fjord, Sweden Core GA113-2Ab
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts ?Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spiny] Gymnodinium catenatum Polykrikos schwartzii
RH434 RH435 RH436 RH437 RH438 RH439 RH440 RH441 RH442 RH443 RH444 RH445 RH446 RH447 RH448 RH449 RH450 RH451 RH452 RH453 0.21
0.22
0.23
0.24
0.25
0.26
0.27
0.28
0.29
0.3
0.31
0.32
0.33
0.34
0.35
0.36
0.37
0.38
0.39
0.4
0 1 59 1 109 9 0 1 0 0 0 25
0 2 45 0 35 2 0 0 0 0 1 16
0 0 26 0 32 2 3 0 0 1 0 13
0 1 37 0 52 9 2 3 0 3 0 10
0 2 93 1 58 3 0 0 0 5 2 18
0 2 65 0 44 6 0 3 0 2 2 16
0 0 34 0 55 4 0 4 0 0 1 12
0 1 88 0 75 6 0 3 0 2 3 19
0 7 62 0 50 6 0 1 0 1 0 16
0 0 54 0 49 4 0 1 0 0 0 16
0 0 96 0 71 2 0 5 0 3 0 13
1 7 77 0 107 8 0 5 0 0 1 32
0 6 112 0 70 2 0 2 0 1 0 28
0 3 73 0 52 1 1 5 0 0 0 16
0 9 119 0 75 5 4 2 0 1 0 30
0 4 118 0 69 7 1 1 0 0 0 20
0 2 97 0 66 5 0 9 0 0 0 30
0 11 124 0 71 4 1 5 0 2 0 29
0 5 69 0 54 5 0 1 0 0 0 17
0 10 166 0 90 7 0 8 0 2 0 36
3
4
1
0
8
13
0
0
0
0
0
0
0
0
0
0
1
2
1
2
12 0 0 0 0 0 9 0 0 0 2 0 0 0 0 192 1
4 0 0 0 0 0 2 0 0 1 0 0 0 0 0 61 4
1 0 0 0 0 1 6 0 0 0 0 0 0 0 0 60 2
4 0 0 0 0 2 8 0 0 0 2 0 0 0 0 89 1
8 0 1 0 0 0 5 0 0 3 2 1 0 0 0 74 2
3 0 0 0 1 0 6 0 0 2 5 0 1 0 0 71 1
3 0 0 0 0 2 13 0 0 0 1 0 3 1 0 62 0
4 0 1 0 0 1 14 0 0 2 4 0 0 1 0 86 0
1 0 0 0 1 0 9 0 1 0 2 1 0 0 1 56 1
4 0 0 0 0 0 8 2 0 1 1 0 1 0 2 54 0
5 0 1 0 0 0 7 0 1 0 1 0 0 0 2 69 1
1 0 1 0 0 0 19 1 0 0 3 0 1 0 3 119 1
2 0 3 0 2 0 7 2 0 1 0 0 0 0 1 70 1
2 0 1 0 0 0 11 1 0 0 0 0 0 0 0 44 1
0 0 0 0 0 0 14 0 0 1 1 1 0 3 4 69 0
0 0 0 0 1 0 17 1 0 0 1 0 0 0 2 89 2
1 0 0 0 0 1 14 0 1 2 0 0 0 0 2 88 0
1 0 0 0 0 0 18 1 1 3 1 0 0 0 5 91 1
0 0 2 0 0 0 8 0 0 1 2 0 2 0 0 76 1
4 0 1 0 0 0 11 0 0 3 5 1 0 0 9 103 1
0 12 22
0 2 5
0 1 5
0 0 8
0 4 12
0 0 10
0 3 2
0 7 7
0 0 5
0 2 2
0 3 5
0 6 1
0 4 3
0 3 1
0 6 2
0 9 2
0 8 6
0 6 2
0 10 2
0 3 1
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Raw counts
Gullmar Fjord, Sweden Core GA113-2Ab Raw counts
0.42
0.43
0.44
0.45
0.46
0.47
0.48
0.49
0.5
0.51
0.52
0.53
0.54
0.55
0.56
0.57
0.58
0.59
0.6
0 10 108 0 60 4 0 2 0 0 4 22
0 4 94 0 86 2 0 4 0 8 0 15
0 14 107 0 140 1 0 3 0 0 3 29
0 8 89 0 96 5 0 3 0 2 0 24
1 6 149 0 118 6 1 4 0 1 0 23
0 2 92 0 70 3 1 2 1 0 0 17
0 10 146 0 120 3 0 7 0 3 0 30
0 10 151 0 108 5 0 3 0 0 0 27
0 3 136 0 90 4 3 2 2 0 0 38
0 3 90 0 110 0 3 1 0 0 0 24
0 9 44 0 117 0 0 0 0 0 0 30
0 3 34 0 78 1 1 1 0 0 0 19
0 12 49 0 89 0 1 1 0 1 0 13
0 5 26 0 85 0 0 2 0 0 0 11
0 23 28 0 125 3 2 5 0 0 1 25
0 5 20 0 52 2 0 1 0 0 0 8
0 6 14 0 92 0 1 0 0 2 0 20
0 6 35 0 119 0 1 3 0 3 0 21
0 9 24 0 69 0 0 2 0 4 0 14
0 6 16 0 87 1 1 4 0 0 0 17
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
5 0 0 0 2 0 9 0 0 0 4 0 0 0 6 77 1
3 0 2 0 0 0 4 0 1 2 4 0 2 2 6 122 19
7 0 0 0 0 2 15 0 2 0 4 0 0 1 2 144 1
0 0 0 0 1 0 7 0 0 0 0 0 0 0 7 99 0
7 0 0 0 2 1 10 0 0 1 6 0 0 1 3 134 3
7 0 1 0 0 0 9 1 0 0 1 0 0 1 1 110 0
4 0 1 0 0 1 14 0 0 0 4 1 1 0 3 145 0
4 0 4 0 2 0 15 0 0 1 0 0 0 0 3 156 0
9 0 3 0 0 0 10 0 1 0 3 0 0 0 2 157 0
5 0 2 0 0 4 13 0 0 1 3 0 0 1 3 148 0
16 0 2 0 0 3 26 1 0 2 3 0 0 0 0 170 0
8 0 1 0 1 4 29 0 0 0 0 0 0 1 1 150 0
7 0 0 0 0 1 24 0 0 1 2 0 0 1 3 168 0
5 0 0 0 2 6 5 0 2 0 0 0 1 1 2 114 0
5 1 3 0 2 0 9 0 3 0 4 0 0 0 1 148 0
6 0 2 0 0 3 4 0 1 0 1 0 0 0 1 62 0
7 1 3 0 1 6 9 0 1 0 2 1 0 0 0 142 3
11 0 1 0 2 4 13 0 1 0 5 0 0 0 0 146 0
3 0 0 0 0 0 5 0 0 0 4 1 0 0 3 65 1
4 0 2 0 0 4 7 0 0 0 2 0 1 1 2 90 0
0 6 8 328
0 8 3 386
0 19 8 502
0 12 4 357
0 24 5 506
0 5 7 331
0 13 5 511
0 6 3 498
0 11 3 477
0 14 2 427
0 18 4 445
0 11 5 348
0 20 4 397
2 9 9 291
9 17 10 424
1 10 1 180
4 14 1 330
5 18 6 400
0 11 1 216
0 11 3 259
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts ?Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spiny] Gymnodinium catenatum Polykrikos schwartzii n
RH454 RH455 RH456 RH457 RH458 RH459 RH460 RH461 RH462 RH463 RH464 RH465 RH466 RH467 RH468 RH469 RH470 RH471 RH472 RH473 0.41
213
214
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graphical data in Figs. 3 and 6, but the larger part of the data sets were divided into two periods, a spring period (March, April and May) and a late summer–autumn (July, August and September) (Figs. 4 and 5). 3.2.2.1. Alsba¨ck series. Despite the Alsb7ck data being the longest period of monitoring for the area there are gaps in the data set. During the early part of the 20th century, salinity and temperature were measured intermittently and it was not until 1958 that measurements became more frequent and dissolved inorganic phosphate (PO4-P) became one of the measured variables. During the late 1960s and in the 1970s dissolved inorganic nitrogen (DIN, sum of NO3, NO2 and NH4) also started to be monitored and in 1980 the measuring frequency became monthly. Unfortunately since 1991 no measurements are taken on the surface water of the fjord within the monitoring programme of this station. This contribution presents all temperature and salinity data for the spring, and late summer– autumn periods, between the years 1890 and 1991 but the data were not averaged because of the varying measuring frequencies. Also presented are the available data sets for PO4 and DIN. The location of the monitoring station is indicated in Fig. 1. These data are available from the Swedish Meteorological and Hydrological Institute (SMHI) and the Water Quality Association of the Bohus Coast (BVVF); hydrographic data before 1958 are from Engstro¨m (1970). 3.2.2.2. Borno¨ series. The Borno¨ series is a unique data set for the Swedish west coast, consisting of daily measurements between the years 1931 and 1989, except Sundays and holidays, of salinity and temperature from eight depths within the water column of Gullmar Fjord. Since the data set is so densely sampled the averages have been calculated for both the spring and late summer/autumn time periods. Further details of this remarkable data series are published in Bjo¨rk and Nordberg (2003) and Arneborg (2004). The location of the Borno¨ sampling station is indicated in Fig. 1. 3.2.2.3. Upwelling events. The upwelling events were calculated using geostrophic wind data. The upwell-
ing event series (Figs. 3–5) was supplied by Bjo¨rk and Nordberg (2003) who should also be consulted for details of their data handling and calculations. 3.2.2.4. Air temperature and precipitation data from Vinga Island. Vinga Island is situated some 10 km west of Go¨teborg (Fig. 1) and air temperature and precipitation were measured daily from 1860 (temperature) and 1879 (precipitation) until 1997 when the station was closed. We present the temperature averages over March to May and July to September (Figs. 4 and 5) and annual precipitation between the years 1890 and 1997, together with the annual precipitation data from Lysekil, between the years 1973 and 2000 (Fig. 3). 3.2.2.5. NAO index. The North Atlantic Oscillation (NAO) has a pronounced effect on the winter climate in Scandinavia (Chen and Hellstro¨ m, 1999). To quantify the NAO, a simple pressure index can be derived from the normalized sea level pressure difference between the Icelandic low and the Azores high (Hurrell, 1995). The NAO index provided herein is the same as that presented by Hurrell (1995) and on the web page http:// www.cgd.ucar.edu/~jhurrell/nao.stat.other.html. The index is averaged over the three winter months January to March and is presented together with a three year running mean (Fig. 3). 3.2.2.6. Primary productivity. Primary productivity is shown in Fig. 6, and has been measured in the fjord using both the 14C technique and the chlorophyll a concentrations. The 14C measurements were taken at Sl7ggo¨, towards the mouth of the fjord (Fig. 1) and the chlorophyll a measurements were taken from the inner part of the fjord (Fig. 1). The 14C data is redrawn from Lindahl et al. (2003); details regarding the 14C method are provided in Lindahl et al. (1998, 2003). The chlorophyll a data are from the Swedish Meteorological and Hydrological Institute (SMHI) and Water Quality Association of the Bohus Coast (BVVF).
4. Results Dinoflagellate cysts were recovered from all the sampled horizons throughout the uppermost 60 cm of
Table 2 Dinoflagellate cyst analysis as calculated cysts per gram of sediment Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09
0.1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19
0.2
0.21
0 0 6 0 51 26 0 0 0 0 0 58
0 64 32 0 1024 112 0 0 0 0 0 144
0 32 96 0 1024 0 0 48 0 0 0 144
0 48 192 0 656 16 0 0 0 0 0 48
0 80 0 0 784 64 0 16 0 0 0 144
0 0 0 0 992 48 0 16 0 0 0 128
16 0 64 0 848 48 0 0 0 0 0 160
0 0 96 0 528 16 0 16 0 0 16 80
0 0 0 0 576 48 0 80 0 0 16 176
0 0 80 0 1200 80 16 0 0 0 0 224
0 32 0 0 1648 96 0 16 0 0 0 144
16 0 16 0 880 80 0 32 0 0 0 160
0 0 32 0 688 144 0 32 0 0 0 160
0 0 112 0 912 48 0 16 0 0 32 144
0 16 16 0 656 160 0 0 0 0 0 288
32 0 0 0 528 240 0 16 0 0 16 208
0 16 208 0 960 208 16 32 0 0 32 304
0 16 176 0 656 112 0 32 0 16 0 272
0 48 336 0 496 160 32 48 0 0 0 208
0 32 176 0 944 32 0 0 0 0 0 112
0 16 944 16 1744 144 0 16 0 0 0 400
0
32
0
64
80
224
64
96
192
176
32
80
0
32
0
0
48
48
48
32
48
6 0 0 0 0 32 77 0 0 6 6 0 0 0 0 666 0
32 0 0 16 0 48 144 0 0 48 48 48 0 0 0 2112 0
48 0 0 32 0 0 160 0 0 0 0 0 48 0 0 1792 32
144 0 4 0 0 96 176 0 0 16 48 32 0 16 0 2096 48
656 0 16 16 48 48 240 8 0 16 32 0 16 0 0 4016 120
448 0 16 0 0 48 368 0 16 0 96 16 0 0 0 4016 64
208 0 0 0 16 80 176 0 0 32 64 0 0 0 0 2496 64
112 0 16 0 0 0 80 0 0 16 48 0 0 0 0 1344 16
96 0 0 0 0 64 240 0 0 0 48 16 0 0 0 1536 32
48 0 0 0 0 96 160 16 0 0 32 16 0 16 0 1904 64
16 0 16 0 0 32 144 0 0 32 32 0 0 0 0 2048 96
144 0 0 0 16 80 272 0 16 16 32 0 16 0 0 2784 16
16 0 0 0 0 16 112 0 0 0 80 16 32 0 0 1632 48
112 0 0 0 0 80 400 0 0 48 32 32 16 0 32 2512 64
32 0 48 0 0 16 224 0 0 48 48 0 0 0 0 2624 96
48 0 64 0 32 0 304 0 16 16 112 16 48 0 0 2976 112
48 0 48 0 0 32 256 0 16 16 64 0 16 32 0 2176 48
64 0 0 0 48 32 164 0 0 0 0 0 16 0 0 1584 64
64 0 0 0 0 32 96 0 16 16 0 0 0 0 0 1056 0
0 0 0 0 0 0 144 0 0 48 0 0 0 0 0 1344 48
192 0 0 0 0 0 144 0 0 0 32 0 0 0 0 3072 16
0 38 32 1005 141 787 5.58 0.75
0 80 128 4112 1408 2464 1.75 0.24
0 32 48 3536 1344 2064 1.54 0.19
0 192 96 3968 1024 2532 2.47 0.39
0 336 128 6832 1168 4576 3.92 0.59
0 64 144 6704 1408 4640 3.30 0.52
0 32 128 4496 1200 2928 2.44 0.39
0 80 64 2640 848 1520 1.79 0.25
0 176 208 3504 1088 1936 1.78 0.25
0 160 112 4400 1776 2304 1.30 0.11
0 160 144 4688 1968 2400 1.22 0.09
0 176 224 5056 1264 3248 2.57 0.41
0 144 32 3184 1056 1936 1.83 0.26
0 144 128 4896 1296 3216 2.48 0.39
0 176 304 4752 1136 3104 2.73 0.44
0 144 272 5248 1040 3696 3.55 0.55
0 80 160 4816 1824 2704 1.48 0.17
0 64 240 3600 1328 1908 1.44 0.16
0 0 368 3008 1376 1216 0.88 0.05
0 80 80 3072 1328 1584 1.19 0.08
0 192 352 7328 3328 3264 0.98 0.01
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio Log H:A Ratio
RH414 RH415 RH416 RH417 RH418 RH419 RH420 RH421 RH422 RH423 RH424 RH425 RH426 RH427 RH428 RH429 RH430 RH431 RH432 RH433 RH434 0.01 m
(continued on next page)
215
216
Table 2 (continued) Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
0.23
0.24
0.25
0.26
0.27
0.28
0.29
0.3
0.31
0.32
0.33
0.34
0.35
0.36
0.37
0.38
0.39
0.4
0.41
0.42
0 32 720 0 560 32 0 0 0 0 16 256
0 0 416 0 512 32 48 0 0 16 0 208
0 16 592 0 832 144 32 48 0 48 0 160
0 32 1488 16 928 48 0 0 0 80 32 288
0 32 1040 0 704 96 0 48 0 32 32 256
0 0 544 0 880 64 0 64 0 0 16 192
0 16 1408 0 1200 96 0 48 0 32 48 304
0 112 992 0 800 0 0 16 0 16 0 256
0 0 864 0 784 64 0 16 0 0 0 256
0 0 1536 0 1136 32 0 80 0 48 0 208
16 112 1232 0 1712 128 0 80 0 0 16 512
0 96 1792 0 1120 32 0 32 0 16 0 448
0 48 1168 0 832 16 16 80 0 0 0 256
0 144 1904 0 1200 80 64 32 0 16 0 480
0 64 1888 0 1104 112 16 16 0 0 0 320
0 32 1552 0 1056 80 0 144 0 0 0 480
0 176 1984 0 1136 64 16 80 0 32 0 464
0 80 1104 0 864 80 0 16 0 0 0 272
0 160 2656 0 1440 112 0 128 0 32 0 576
0 160 1728 0 960 64 0 32 0 0 64 352
0 64 1504 0 1376 32 0 64 0 64 0 240
64
16
0
128
208
0
0
0
0
0
0
0
0
0
0
16
32
16
32
0
0
64 0 0 0 0 0 32 0 0 16 0 0 0 0 0 976 64
16 0 0 0 0 16 96 0 0 0 0 0 0 0 0 960 32
64 0 0 0 0 32 128 0 0 0 32 0 0 0 0 1424 16
128 0 16 0 0 0 80 0 0 48 32 16 0 0 0 1184 32
48 0 0 0 16 0 96 0 0 32 80 0 16 0 0 1136 16
48 0 0 0 0 32 208 0 0 0 16 0 48 16 0 992 0
64 0 16 0 0 16 224 0 0 32 64 0 0 16 0 1376 0
16 0 0 0 16 0 144 0 16 0 32 16 0 0 16 896 16
64 0 0 0 0 0 128 32 0 16 16 0 16 0 32 864 0
80 0 16 0 0 0 112 0 16 0 16 0 0 0 32 1104 16
16 0 16 0 0 0 304 16 0 0 48 0 16 0 48 1904 16
32 0 48 0 32 0 112 32 0 16 0 0 0 0 16 1120 16
32 0 16 0 0 0 176 16 0 0 0 0 0 0 0 704 16
0 0 0 0 0 0 224 0 0 16 16 16 0 48 64 1104 0
0 0 0 0 16 0 272 16 0 0 16 0 0 0 32 1424 32
16 0 0 0 0 16 224 0 16 32 0 0 0 0 32 1408 0
16 0 0 0 0 0 288 16 16 48 16 0 0 0 80 1456 16
0 0 32 0 0 0 128 0 0 16 32 0 32 0 0 1216 16
64 0 16 0 0 0 176 0 0 48 80 16 0 0 144 1648 16
80 0 0 0 32 0 144 0 0 0 64 0 0 0 96 1232 16
48 0 32 0 0 0 304 0 16 32 64 0 32 32 48 1952 96
0 32 80 2944 1680 1088 0.65
0 16 80 2464 1248 1104 0.88
0 0 128 3696 1872 1632 0.87
0 64 192 4832 3040 1408 0.46
0 0 160 4048 2448 1392 0.57
0 48 32 3200 1760 1312 0.75
0 112 112 5184 3152 1744 0.55
0 0 80 3440 2192 1152 0.53
0 32 32 3216 1984 1104 0.56
0 48 80 4560 3040 1312 0.43
0 96 16 6304 3808 2368 0.62
0 64 48 5072 3536 1392 0.39
0 48 16 3440 2416 928 0.38
0 96 32 5536 3920 1488 0.38
0 144 32 5504 3520 1808 0.51
0 128 96 5328 3360 1728 0.51
0 96 32 6064 3984 1936 0.49
0 160 32 4096 2432 1472 0.61
0 48 16 7408 5136 2144 0.42
0 96 128 5248 3360 1584 0.47
0 128 48 6176 3344 2608 0.78
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio
RH435 RH436 RH437 RH438 RH439 RH440 RH441 RH442 RH443 RH444 RH445 RH446 RH447 RH448 RH449 RH450 RH451 RH452 RH453 RH454 RH455 0.22
Gullmar Fjord, Sweden Core GA113-2Ab Cysts per gram of sediment
RH457
RH458
RH459
RH460
RH461
RH462
RH463
RH464
RH465
RH466
RH467
RH468
RH469
RH470
RH471
RH472
RH473
0.44
0.45
0.46
0.47
0.48
0.49
0.5
0.51
0.52
0.53
0.54
0.55
0.56
0.57
0.58
0.59
0.6
0 224 1712 0 2240 16 0 48 0 0 48 464
0 128 1424 0 1536 80 0 48 0 32 0 400
16 96 2384 0 1888 96 16 64 0 16 0 368
0 32 1472 0 1120 48 16 32 16 0 0 272
0 160 2336 0 1920 48 0 112 0 48 0 480
0 160 2416 0 1728 80 0 48 0 0 0 432
0 48 2176 0 1440 64 48 32 32 0 0 608
0 48 1440 0 1760 0 48 16 0 0 0 384
0 144 704 0 1872 0 0 0 0 0 0 480
0 48 544 0 1248 16 16 16 0 0 0 304
0 192 784 0 1424 0 16 16 0 16 0 208
0 80 416 0 1360 0 0 32 0 0 0 176
0 368 448 0 2000 48 32 80 0 0 16 400
0 80 320 0 832 32 0 16 0 0 0 128
0 96 224 0 1472 0 16 0 0 32 0 320
0 96 560 0 1904 0 16 48 0 48 0 336
0 144 384 0 1104 0 0 32 0 64 0 224
0 96 256 0 1392 16 16 64 0 0 0 272
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
112 0 0 0 0 32 240 0 32 0 64 0 0 16 32 2304 16
0 0 0 0 16 0 112 0 0 0 0 0 0 0 112 1584 0
112 0 0 0 32 16 160 0 0 16 96 0 0 16 48 2144 48
112 0 16 0 0 0 144 16 0 0 16 0 0 16 16 1760 0
64 0 16 0 0 16 224 0 0 0 64 16 16 0 48 2320 0
64 0 64 0 32 0 240 0 0 16 0 0 0 0 48 2496 0
144 0 48 0 0 0 160 0 16 0 48 0 0 0 32 2512 0
80 0 32 0 0 64 208 0 0 16 48 0 0 16 48 2368 0
256 0 32 0 0 48 416 16 0 32 48 0 0 0 0 2720 0
128 0 16 0 16 64 464 0 0 0 0 0 0 16 16 2400 0
112 0 0 0 0 16 384 0 0 16 32 0 0 16 48 2688 0
80 0 0 0 32 96 80 0 32 0 0 0 16 16 32 1824 0
80 16 48 0 32 0 144 0 48 0 64 0 0 0 16 2368 0
96 0 32 0 0 48 64 0 16 0 16 0 0 0 16 992 0
112 16 48 0 16 96 144 0 16 0 32 16 0 0 0 2272 32
176 0 16 0 32 64 208 0 16 0 80 0 0 0 0 2336 0
16 0 0 0 0 0 80 0 0 0 64 16 0 0 48 1040 16
64 0 32 0 0 64 112 0 0 0 32 0 16 16 32 1440 0
0 304 128 8032 4752 2736 0.58 0.24
0 192 64 5712 3648 1824 0.50 0.30
0 384 80 8096 4944 2576 0.52 0.28
0 80 112 5296 3008 1984 0.66 0.18
0 208 80 8176 5104 2720 0.53 0.27
0 96 48 7968 4864 2896 0.60 0.23
0 176 48 7632 4448 2816 0.63 0.20
0 224 32 6832 3696 2800 0.76 0.12
0 288 64 7120 3200 3312 1.04 0.01
0 176 80 5568 2192 2992 1.36 0.14
0 320 64 6352 2656 3200 1.20 0.08
96 144 144 4656 2064 2224 1.08 0.03
144 272 160 6784 3392 2880 0.85 0.07
16 160 16 2880 1408 1200 0.85 0.07
80 224 16 5280 2160 2768 1.28 0.11
80 288 96 6400 3008 2832 0.94 0.03
0 176 16 3424 1952 1264 0.65 0.19
0 176 48 4144 2112 1744 0.83 0.08
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Gonyaulacacean cysts Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Nematosphaeropsis labyrinthus Protoceratium reticulatum Spiniferites bentorii Spiniferites delicatus Spiniferites elongatus Spiniferites lazus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet. Peridiniacean cysts Pentapharsodinium dalei Protoperidiniacean cysts Islandinium cf. cesare Lejeunecysta marieae Lejeunecysta oliva Protoperidinium avellana Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum/nudum Protoperidinium compressum Protoperidinium divaricatum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [P] Protoperidinium spp. indet. [RB] Protoperidinium sp. nov. Gymnodinialean cysts Cyst nov. [sparse spines] Gymnodinium catenatum Polykrikos schwartzii Total cysts per gram Autotrophs Heterotrophs H:A Ratio Log H:A Ratio
RH456 0.43
217
218
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
Core GA113-2Ab. The quantitative data are provided in Tables 1 and 2. In addition the samples contained bisaccate and angiosperm pollen together with copepod egg cases, foraminiferal linings and much structured and amorphous organic material. The numerical data, in particular the numbers of cysts per gram of sediment of selected species, have been used to construct the dinoflagellate cyst spectrum illustrated in Fig. 2. The cyst spectrum clearly demonstrates a number of features that are of note. Firstly it can be seen that the dinoflagellate cysts are well represented throughout the core, generally occurring at about the 4000 cysts per gram level but sometimes rising to over 7000 cysts per gram of sediment. These figures are much higher than those recorded for sediments preserved in Koljo¨ Fjord (Harland et al., 2004a) but are reasonably close to the figure recorded by Persson et al. (2000) of 11,000 from Alsb7ck, Gullmar Fjord. It is also clear that the Gullmar Fjord sediments contain higher numbers of gonyaulacacean cysts (up to 5000 cyst per gram) than those in neighbouring Koljo¨ Fjord (no more than 2000 cysts per gram), which undoubtedly reflects the more restricted nature of the water mass in the latter fjord. Indeed the fact that the accumulation rate in Gullmar Fjord is at least twice that in Koljo¨ Fjord (0.6–1.4 cm y 1 as opposed to 0.4 cm y 1) (Filipsson and Nordberg, 2004 and Nordberg et al., 2001), further accentuates the difference. It is interesting to note the presence of Ataxiodinium choane, Bitectatodinium tepikiense, Nematosphaeripsis labyrinthus, Protoceratium reticulatum and Spiniferites mirabilis within the Gullmar Fjord dataset, in contrast to Koljo¨ Fjord, as possible indicators of more open marine environments. Indeed all these species are known to occur in the Zone 1 assemblage of Dale (1985) of a core taken in the Skagerrak, which is also comparable with the present day cyst flora from the coastal waters of southern and western Norway (Grøsfjeld and Harland, 2001). In many respects the cyst spectrum from Gullmar Fjord is much less variable than that of Koljo¨ Fjord, in both cyst numbers and the record of individual cyst species, and consequently allows for less differentiation. This fact is also reflected in the nature of the sediment record i.e. the homogeneous organic rich clay of Gullmar Fjord versus the occurrence of discrete
intervals of laminated sediments within the Koljo¨ Fjord sequence. These observations are in accord with the geography and hydrography of Gullmar Fjord whose response to the environmental signal appears to be rather less complicated than the other more restricted fjords along the Swedish west coast. In particular the Gullmar Fjord dinoflagellate cyst spectrum can be divided into two major units as demonstrated from a visual inspection of the dinoflagellate cyst spectrum (Fig. 2), the stratigraphically constrained cluster analysis and the heterotrophic ratio (Fig. 3). These consist of an upper Unit I and a lower Unit II. However it is possible that the lower unit may also be further subdivided into three minor units. The two major units are described below: Unit I: 0.01–0.21 m; deposited between the years 1969 and 1999; this youngest unit within the sequence is characterised by a relatively high diversity of twenty-nine cyst species and over 3000 cysts per gram of sediment. In particular it contains high numbers of Protoceratium reticulatum, Spiniferites bentorii, ?Pentapharsodinium dalei, Protoperidinium avellana, Protoperidinium conicoides, Protoperidinium conicum, Protoperidinium pentagonum, Protoperidinium spp. [spiny], Islandinium cf. cesare and Polykrikos schwartzii. The particular presence of S. bentorii is perhaps indicative of a specific salinity regime possibly similar to those pertaining in the Irish Sea or indeed to seasonal localised salinity and temperature conditions (see Reid, 1974); it is not uncommon along the west coast of Sweden (Persson et al., 2000) and also in the latest Holocene sediments from Koljo¨ Fjord (Harland et al., 2004a). However it is likely that the environmental reasons for its presence are both complex and dynamic, and perhaps some seasonal overprinting has occurred as indicated by the inverse relationship between this cyst species and ?Pentapharsodinium dalei (Fig. 2), which tend to be late summer/autumn and spring/early summer species, respectively. Interestingly the other well known late summer/autumn species, Lingulodinium polyedra, is notable by its low numbers and is, therefore, not reacting to the changing environment in the same way as the other two species. The sampling is of sufficient frequency that seasonal differences will impinge upon the recovered assemblages. The log H : A ratio (Fig. 3) is within positive values throughout Unit I and reflects the high
R. Harland et al. / Science of the Total Environment 355 (2006) 204–231
numbers of heterotrophic dinoflagellates present and the decline in the numbers of gonyaulacacean cysts (see also Fig. 2). Reduced frequencies of water exchanges/turnover or complete water renewal is part of a likely explanation because of the positive nature of the NAO, i.e. the increase of moisture laden westerly winds in the winter driving less saline waters towards the Swedish coast and effectively strengthening the pycnocline and acting to stabilise the water column (Nordberg et al., 2001; Bjo¨rk and Nordberg, 2003; Filipsson and Nordberg, 2004). The stability of the water column may also be reflected by the higher numbers of Spiniferites bentorii, a particular indicator of cyst production in stable and stratified late summer conditions. This dinoflagellate cyst unit is, in part, correlatable to the upper foraminiferal zone identified by Nordberg et al. (2000) and Filipsson and Nordberg (2004), indicative of declining oxygen concentrations in the bottom water and together with mostly positive NAO values, which decrease the potential for upwelling events within the Skagerrak. Parallels with the results from Koljo¨ Fjord are also evident in that its unit I, dated between 1980 and 1998, is also linked to lower bottom water salinity (Nordberg et al., 2001). Unit II: 0.22–0.60 m; deposited between the years 1915 and 1969; this older unit within the sequence is characterised by a high diversity of thirty-one species and over 4000 cysts per gram of sediment. In particular this major unit contains high proportions of Bitectatodinium tepikiense, Lingulodinium polyedrum, Spiniferites elongatus, Spiniferites mirabilis and peridinioid Protoperidinium species. The higher proportions of both B. tepikiense and L. polyedrum together with the reduction of S. bentorii are evidence of a possible salinity change and seasonal differences (see Reid, 1974). However the exact nature of these changes is difficult to establish. Rochon et al. (1999) provided histograms of the mean relative abundance of various taxa as calculated for given intervals of salinity and other physical parameters. These data suggest that B. tepikiense is most abundant at salinities (August) between 27x–36x and L. polyedrum between salinities 30x–36x, in contrast to S. bentorii, which is most abundant between salinities 34x–36x. A suggested inter-
219
pretation is, therefore, that Unit II may be indicative of somewhat different salinities to Unit I but that these differences are difficult to identify and quantify. The log H : A ratio (Fig. 3), in contrast to Unit I, is within negative values and therefore indicates that there are relatively more autotrophic dinoflagellates than heterotrophic dinoflagellates, as expressed in the cyst record from the numbers of gonyaulacacean cysts. It also evident from the H : A ratio that the lowermost part of Unit II returns to positive values (Fig. 3) suggesting other changes have occurred within the environment of deposition during this time. Undoubtedly changes occurring within the sequence are many and complex involving salinity, nutrient availability and other factors. Some of these other factors will remain unknown until there is better knowledge of the ecology of dinoflagellates and their cysts. This part of the sequence in Gullmar Fjord is largely correlatable to the lower foraminiferal zone as first described by Nordberg et al. (2000) and detailed from the corresponding core by Filipsson and Nordberg (2004). It is also correlatable to mostly negative NAO values, which are indicative of a greater potential for upwelling events along the coast. In addition to the two major units the second unit may be further subdivided into the three minor units described below: a) 0.22–0.31 m; deposited between the years 1955 and 1969; characterised by low Bitectatodinium tepikiense, relatively low Lingulodinium polyedrum, relatively low Spiniferites elongatus, low Gymnodinium catenatum and relatively high Polykrikos schwartzii. b) 0.32–0.49 m; deposited between the years 1928 and 1955; characterised by high Bitectatodinium tepikiense, high Lingulodinium polyedrum, high Spiniferites elongatus, high Gymnodinium catenatum and relatively low Polykrikos schwartzii. c) 0.50–0.60 m; deposited between the years 1928 and 1915; characterised by high Bitectatodinium tepikiense, low Lingulodinium polyedrum, low Spiniferites bentorii, low S. elongatus, and high numbers of Protoperidinium conicoides, high Gymnodinium catenatum and low Polykrikos schwartzii.
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The full extent and significance of these fluctuations within the dinoflagellate cyst spectrum must await further consideration in the light of other evidence and not withstanding the lack of good and reliable autecological data.
5. Comparisons with other long term datasets As a part of this study, and to gain some insight into the changing environmental parameters through this 85-year temporal period, a series of hydrographical and historical records were consulted (see Materials and methods). The results from these are noted below and compared to the cyst record in order to gain a better understanding of the complex and dynamic system of which the dinoflagellate cyst record is only a tiny part. We believe that in so doing the relationship between the dinoflagellate cysts and hydrography, often used as a proxy for various parameters, will be available for examination within this high-resolution temporal record. 5.1. Hydrographical information In order to test the applicability of using certain cyst types as proxies for various environmental parameters, including cultural eutrophication, and taking advantage of the unique time series of hydrographical measurements available for Gullmar Fjord a series of graphs are provided herein (Figs. 3–6). These graphs variously examine the dinoflagellate cyst record against the water temperature at Alsb7ck and Borno¨; salinity at Alsb7ck and Borno¨; productivity in terms chlorophyll a and the amount of mgC m 2d 1 together with the amount of such nutrients as DIN and PO4-P; upwelling; precipitation and the air temperature at Vinga. The dinoflagellate cyst forming species commonly occurring along the west coast (Persson et al., 2000; Godhe and McQuoid, 2003) and identified as ecologically meaningful and easily identifiable include Lingulodinium polyedrum, Spiniferites bentorii, Pentapharsodinium dalei and the total number of protoperidiniacean cysts; these species were discussed in some detail in Harland et al. (2004a) and have recently been reviewed by Marret and Zonneveld (2003). In addition the total number of cysts per gram
and the heterotrophic ratio are also provided as these parameters have also been used controversially as environmental proxies (Matsuoka, 1999, 2001; Dale, 2001). The hydrographical parameters chosen to compare with the cyst record are those usually quoted in the literature as being important in the distribution of dinoflagellate cysts in bottom sediments from the marine realm. These are temperature; salinity; PO4 and DIN as a measure of nutrient availability. Plotting these various parameters in the temporal domain is less circumstantial herein than some earlier studies where the cyst records have been plotted only against an interpretation of environmental events (Dale et al., 1999). It is essential that if dinoflagellate cysts are to be used as proxies for any of the environmental parameters, including the examination of eutrophication, then the variance in their temporal record must be set against measured hydrographical variables as a test of the methodology before any confidence can be placed in their utility. The following section examines the cyst record against these various hydrographical parameters. The first of the four figures (Fig. 3), detailing the various hydrographical parameters, includes the total number of cysts per gram of sediment, the total number of protoperidiniacean cysts and the log heterotrophic ratio with the NAO index, the upwelling record and precipitation. Perusal of the diagram reveals the prominence of the change at around 1969/1970 with the increase in protoperidiniacean cysts reflected in the higher heterotrophic ratio together with the movement of the NAO into positive values and the reduction in the number of upwelling events. This correlation was noted earlier in the Results Section. A second figure (Fig. 4) examines the occurrence of the dinoflagellate cyst species, seasonally produced during the spring, against the hydrographical parameters of water temperature, salinity, upwelling frequencies and air temperature. The record of Pentapharsodinium dalei and the total protoperidiniacean cyst curve reveals increased numbers post 1970, although additionally the former does show increased numbers somewhat earlier around 1961. The spring records of the hydrographic parameters shows little differentiation except perhaps for a falling salinity trend in the Borno¨ data and a general
NAO index
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Vinga Lysekil
Fig. 3. A series of graphs detailing the total number of cysts per gram of sediment plotted against time (A); the total number of protoperidiniacean cysts per gram of sediment against time (B); the log heterotrophic ratio (C); the NAO index (D); the upwelling record (E); and the precipitation record for Vinga and Lysekil (F). The data collection and all calculations are explained in the text.
lessening of spring upwelling. Indeed the spring dinoflagellate cyst record is behaving similarly to the total cyst record and is in tune to changes within the hydrography of the fjord that has responded to the major change in the NAO i.e. a reduced number of spring upwelling events. In Fig. 5 the two dinoflagellate cysts that are produced during the late summer/autumn, i.e. Lingulodinium polyedrum and Spiniferites bentorii are plotted against the summer surface temperature and
salinity from Alsb7ck and Borno¨. There is little differentiation within the data although there is an indication that summer SST were somewhat higher between 1930 and 1970 and particularly so between 1931 and 1950; this is also seen in the averaged summer air temperatures recorded at Vinga. Using Student’s t-test the difference between the average temperatures between the two periods is statistically significant at the 95% level; hence it was 0.5 8C warmer on average and less variable. This appears to
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Fig. 4. Dinoflagellate cyst and instrumental data for the spring plotted against time and including the spring dbloomerT Pentapharsodinium dalei per gram of sediment (A); the total protoperidiniacean cysts per gram of sediment (B); surface temperatures recorded at Alsb7ck (C) and Bornf (D); surface salinities recorded at Alsb7ck (E) and Bornf (F); the upwelling record (G); and the air temperature at Vinga (H). Data collection and calculations are fully explained in the text.
correspond to the raised numbers of the cysts of Lingulodinium polyedrum between the same years. Indeed the increase in numbers of Lingulodinium polyedrum starts a little earlier in 1928/1929 but
unfortunately the Borno¨ data series does not begin until 1931. The air temperature data from Vinga also reveals higher summer temperatures from about 1924 until about 1958. In addition the histogram of
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S. bentorii (cysts/g) L. polyedra (cysts/g)
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Fig. 5. Dinoflagellate cyst and instrumental data for the summer–autumn plotted against time and including the late summer dbloomersT Lingulodinium polyedrum (A) and Spiniferites bentorii (B). The other graphs are as explained in the previous figure. Data collection and calculations are explained in the text.
upwelling events over the temporal record also shows an increase over these same years. Is it premature to establish a causal link between the two?
Finally Fig. 6 provides the data series for nutrients and primary productivity within the fjord at Alsb7ck and Sl7ggo¨. Unfortunately the records are limited in
PO 4-P (µM)
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Inner part
10 5 0 1985 2500 D 2000 1500 1000 500 0 1985
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¨ go¨ Slag
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Fig. 6. Instrumental data from Gullmar Fjord illustrating the phosphate concentrations in the surface waters at Alsb7ck (A); the dissolved inorganic nitrate concentrations at Alsb7ck (B); the primary production in the inner part of the fjord as expressed in the chl-a concentrations (C); and the primary production as expressed in concentrations of carbon (D). Data collection and calculations are explained in the text. The primary production series clearly shows the annual cyclicity with peaks of production generally in the spring or late summer.
their coverage, from 1960 for the nutrients and 1985 for the primary productivity, but all show little internal differentiation and only a slight increase in nutrients over the period; however there are clearly defined annual phytoplankton cycles as one would expect in these coastal fjord environments. 5.2. Local pollution history In the first half of the 20th century, that is until the mid-1960s, the innermost part of the fjord was strongly affected by industrial pollution from a sulphite pulp mill and untreated sewage outfalls from Munkedal village (Rosenberg, 1976). The pulp mill was active from 1945 to 1966, the year when it finally
closed. After 1966, when both the industrial pollution and sewage had ceased, the water quality in the innermost part of the fjord together with the benthic life recovered surprisingly quickly (Rosenberg, 1976). Beyond the mid-1970s no significant, local pollution sources were present anywhere in the fjord (Lindahl et al., 1998) and discharge from outfalls from the herring canneries and untreated sewage from the small town of Lysekil, towards the outer part of the fjord, and villages along the length of the fjord had ceased following the introduction of sewage treatment plants for both household and industrial waste. Indeed untreated sewage from water closets in Lysekil was at its worst during 1950–1975, when the population of the town was between 7000–8000. At about the same time the local canning industry was active i.e. between 1945 and 1970, with most activity in the 1950s and 1960s; finally coming to a swift decline in the 1970s. The canneries on the fjord shore produced approximately 80% of the total amount of oxygen consuming effluent and nitrogen. Interestingly the various symptoms of large scale eutrophication only began to be reported from the 1970s and 1980s at a time following the treatment of sewage, and the closing of both the Munkedal sulphite pulp mill (1966) and the herring canning industry (1970s) within the fjord.
6. Discussion The dinoflagellate cyst analysis of Core G1132Ab, taken in Gullmar Fjord, has provided one of the most detailed high-resolution records published to date. The resolution of approximately 1.5 years per sample provides a unique opportunity to examine closely the changing surface water environments within this fjord on the west coast of Sweden. It is particularly apt that this record should have been recovered from an area that boasts one of the world’s first oceanographic institutions. The dinoflagellate cyst species recovered are consistent with those recorded from modern sediments along the west coast of Sweden and documented within the literature for the area (Erdtman, 1954; Persson et al., 2000). In particular the presence of the more open marine species (see above) is entirely consistent with the open aspect of Gullmar
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Fjord in comparison to other west coast fjords particularly those that have a more restricted access to Skagerrak waters such as Koljo¨ Fjord (Harland et al., 2004a). Dinoflagellate cyst distribution patterns are largely governed by several factors, with the assumption that there has been no post mortem alteration or other taphonomic interference (see below), notably temperature (36% of the variance following the CCA of Marret and Zonneveld’s 2003 compilation of 835 samples); position within an onshore/offshore gradient (49% of the variance within their dataset); and the availability of nutrients within the surface waters including annual phosphates (33% of the variance) and annual nitrates (32% of the variance). Salinity is a well known determinant in cyst distribution patterns (Dale, 1996), but interestingly it could not be significantly related to the variance within the data of Marret and Zonneveld (2003). The dinoflagellate cyst distribution patterns generally hold true for autotrophic dinoflagellates as well as for the heterotrophs, which are ultimately reliant upon the availability and distribution of autotrophic prey species within the phytoplankton. A recently published paper on the influence of environmental factors on the distribution of cysts along the Swedish west coast (Godhe and McQuoid, 2003) has investigated the effect of 46 parameters using a variety of multivariate statistical methods. The density of the total cyst assemblages from autotrophic dinoflagellates was principally related to surface temperature and the availability of macronutrients and inversely related to the occurrence of competitors within the phytoplankton. Not surprisingly the abundance of heterotrophic dinoflagellate cyst taxa was related to their prey preference. The cyst forming dinoflagellates produce cysts as a natural part of their life cycle seemingly triggered by nutrient depletion following a phase of exponential growth; cysts typically appear in the plankton following the spring phytoplankton bloom and the late summer bloom (Pfiester, 1975; Turpin et al., 1978; Anderson and Lindquist, 1985). Recent work by Godhe et al. (2001) in a Gullmar Fjord suggests that cyst production may occur throughout the dgrowing seasonT as sexual reproduction is maintained and that temperature and light intensity has significant
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influence on cyst production. In contrast, work in Lambert’s Bay, South Africa on Zygabikodinium lenticulatum demonstrates cyst production over a short period with rapid export production through the water column (Joyce and Pitcher, 2004). Particular cyst species appear to have evolved to take advantage of either or both of these phytoplankton growth phases whereas others appear to be more opportunistic (see Harland et al., 2004b and references therein). If we assume that the regional climate has not changed markedly over the last 110 years, as can be demonstrated from the temporal series of such surface water parameters as temperature and salinity, (Figs. 3– 6), to alter significantly the cyst distribution patterns of the region then much of the temporal dinoflagellate cyst record must be attributable to changes in the availability of nutrients, trace elements and other abiotic and biotic factors on seasonal and annual timescales. However it is noteworthy that evidence is growing that recent climate warming has induced a major reorganisation of the North Atlantic pelagic ecosystem from phytoplankton to fish since the late 1980s (Beaugrand et al., 2002) and will undoubtedly impact the North Sea and contiguous waters, including their dinoflagellate flora and consequently cyst production. The availability of nutrients within the water column are variously derived from the coastal hinterland as run-off; from tidal mixing of sediments in the shallow nearshore zone especially during the winter months and around the vernal and autumnal equinoxes; and from upwelling and advection in the offshore areas. The provision of nutrients is, after latitude/temperature, the second most important determinant in phytoplankton and dinoflagellate cyst distribution patterns (see Marret and Zonneveld, 2003). In the context of the Swedish west coast the availability of nutrients to the phytoplankton derives from the surface water circulation pattern and the changing water mass types with their inherent properties of temperature, salinity and nutrient content together with various qualities such as the distribution of trace elements. Tidal energy is low and the effect of run-off is negligible in the more open aspect of Gullmar Fjord (Bjo¨rk and Nordberg, 2003). In this respect the exchange of water with the open sea, the Kattegat and Skagerrak, is all important to marine life
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in the coastal zone (Bjo¨rk and Nordberg, 2003). This water exchange is largely driven by geostrophic winds that have the effect of forcing upwelling and controlling the availability of nutrients within the system. The upwelling history, tuned from a unique longseries hydrographic dataset, suggests a declining trend between the late 1890s and 1920; an increasing frequency to 1940; and a further decline between the 1950s and 1990 (Bjo¨rk and Nordberg, 2003). These upwelling trends are mirrored, in particular, by the Lingulodinium polyedrum curve within the dinoflagellate cyst spectrum. This changing frequency in the availability of nutrients through fluctuations in summer upwelling events may be sufficient to allow such a dinoflagellate like Lingulodinium polyedrum, that thrives in stable and stratified water but can take ecological advantage of increased nutrients from depth, to increase its population size and so on encystment produce increased cyst numbers to enter the fossil record (Marret and Zonneveld, 2003; Harland et al., 2004a). However a temporal record as documented herein is also affected by taphonomic influences, which in the case of dinoflagellate cysts largely involves the availability of oxygen at the sea floor and within the sediments. It is known that certain cyst species are preferentially oxidised in these environments in the presence of oxygen (Zonneveld et al., 1997, 2001) whilst others are less susceptible. In Gullmar Fjord where the bottom sediments are sometimes subject to periods of hypoxia/anoxia, especially after 1980 (Filipsson and Nordberg, 2004), there are some increases in the numbers of protoperidiniacean cysts and the heterotrophic ratio. However the general high level of cyst recovery within the sediments, both of cysts of autotrophic and heterotrophic dinoflagellates, is suggestive that this taphonomic effect is not a problem. More recently Persson and Rosenberg (2003) have reported that dinoflagellate cyst preservation and cyst numbers occurring within bottom sediments are affected by grazing from benthic fauna. In oxygenated bottom waters grazing produced a relative increase in cyst numbers particularly in the species Lingulodinium polyedrum, Protoceratium reticulatum and Spiniferites spp. It is unlikely that this phenomenon would have much effect on the temporal record from Gullmar Fjord with its particularly high cyst recovery
(see above). Nonetheless it is important to be aware of these various taphonomic factors that could bias the fossil record of dinoflagellate cysts. The dinoflagellate cyst record documented from Core GA113-2Ab taken in the Gullmar Fjord appears to be responding to change occurring in the Skagerrak and possibly further afield in the North Sea. The coastal current running up the west coast of Sweden from the Kattegat is highly variable and responds rapidly to changes in the geostrophic wind patterns (Bjo¨rk and Nordberg, 2003). Consequential upwelling resulting from the wind patterns will control the amount of nutrients coming to the surface through advection and Ekman pumping in the offshore area and hence will have a marked effect on the dinoflagellate populations and eventually on the cyst record. The dinoflagellate cyst record detailed herein has a distinctive signature, which points to some environmental change within the marine realm at around 1969/1970. This change involves the decline in the numbers of Bitectatodinium tepikiense, and Lingulodinium polyedrum together with a concomitant increase in numbers of Spiniferites bentorii, Pentapharsodinium dalei and protoperidiniacean cysts. This environmental change is registered within those dinoflagellates producing cysts in both the spring and late summer/autumn. Examination of the various hydrographical parameters, using long sequence high resolution instrumental records, has enabled us to match this change to only two parameters. Interestingly it was not possible to identify any correspondence with temperature, salinity or indeed to nutrient content despite a possible gently rising trend in the nutrients from Alsb7ck. The only reasonable match recognised was between the dinoflagellate cyst record and the frequency of upwelling in coastal waters brought about as a consequence of the action of the NAO. As the NAO changed from a negative phase to a positive phase at around 1972/1973 the frequency of upwelling decreased. This partly corresponds with a statistically significant rise in summer temperatures at Borno¨. It is surprising that such a large and significant change in the dinoflagellate cyst populations is not reflected by a similarly large change in the hydrographic parameters but is seemly corresponding to the large scale reorganisation of the North Atlantic
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climate patterns that is characterised by the NAO. In particular the pattern of occurrence of Lingulodinium polyedrum, often now used as an indicator species for eutrophication (Sangiorgi and Donders, 2004), does not correspond to the nutrient curves or phytoplankton primary production or to the local pollution history within the fjord (see Section 5.2 (Local pollution history)). Indeed problems with large scale eutrophication within the fjord began to be reported in the 1960s interestingly at a time that the Lingulodinium polyedrum curve shows a steady decline in numbers. The simplistic use of this species as an eutrophication indicator is, therefore, not justified by these findings. Indeed our findings rather suggest that the ecology of dinoflagellates within the fjord and coastal water environment is not easily related to simple hydrographic parameters but is rather more complex and dynamic. Recent work has thrown light on the complexity of the ecology of dinoflagellates and their cysts which belies a simplistic approach to the interpretation of the fossil record. In particular our knowledge of the relationship between dinoflagellate productivity, cyst production and distribution is poor. This relationship is, however, vital if we are to link the occurrence of environmental change in surface waters to the record of dinoflagellate cysts within the sediments and more research is desperately needed, especially at a time when dinoflagellate ecology is undergoing revision. Recent research (Smayda, 2002) has pointed out certain inconsistencies in the present dinoflagellate ecological paradigm. The establishment of a stable, stratified water column is usually regarded as necessary for the high productivity of autotrophic dinoflagellates. These dinoflagellates are intolerant to shear stress caused by water mixing or turbulence and they utilise swimming strategies to occupy optimum environments; this relationship has been described using Margalef’s Mandala (see Taylor, 1987, Fig. 11A.4). However the stratification of the water column is least likely to provide nutrients and to initiate high productivity, leading to sexual reproduction and cyst production as the nutrient supply is depleted. Some dinoflagellates such as Pentapharsodinium dalei take advantage of the nutrient inoculum following the winter/spring storms whereas others, such as Lingulodinium polyedrum, favour the summer/early
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autumn. The contradiction of using the latter as an indicator of eutrophication is obvious. We have argued previously (Harland et al., 2004a) that Lingulodinium polyedrum is capable of gathering nutrients, not from an increased supply from cultural eutrophication, but rather from depth as a result of normal hydrographical processes. Smayda and Reynolds (2001, 2003) in their matrix of dinoflagellate life forms classify Lingulodinium polyedrum as a Type V (Upwelling Relaxation Taxa) involving survival strategies that include the secretion of large amounts of mucous to dampen turbulence together with high swimming speeds of 258 to 400 Ams 1 (see Smayda, 2002, Table 1). Such autecological strategies may provide Lingulodinium polyedrum with unique properties that enable it to prosper in these particular circumstances. Most recently Smayda and Reynolds (2003) have discussed the ecological strategies employed by dinoflagellates for survival. Although their discussions focus on the production of harmful algal blooms (HABs) some factors are pertinent to the interpretation of the fossil record. In order to survive dinoflagellates as a group must be able to tolerate high physical disturbance, light stress and nutrient limitations and not only to enjoy optimal conditions but also to cope with less than optimal environments. Adaptive strategies have arisen as a coping mechanism and can be recognised within a number of species associations including C-strategists (competitors), S-strategists (stress tolerant species) and R-strategists (ruderal or disturbance tolerant species). Originally applied to freshwater species (Reynolds, 1988) this concept can be applied to the marine realm (Smayda and Reynolds, 2003) and to the cyst forming dinoflagellates. Indeed many of the cyst forming dinoflagellates are well known in neritic environments and appear to be R-strategists in order to overcome the shear stress associated with turbulence and water mixing often prevalent in these environments. Not withstanding that much of this work stems from the study of HABs the ecology of dinoflagellates is organised around associations of species reacting to abiotic factors of irradiance, nutrients and turbulence with species selected to fulfil one of the strategies described above. This relatively simple plan (the 3-3 plan of Smayda and Reynolds, 2003) will encompass the production of cysts as a part of the ecological expedient to survive neritic environments.
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In the present study the dinoflagellate cyst record is an amalgam of this ecological paradigm as applied to all the species recorded and cannot be regarded as a simple set of curves reacting to simple changes in the environment. We have focused upon Lingulodinium polyedrum as it has and is being used as an indicator of eutrophication and Pentapharsodinium dalei, a cyst most often used to indicate cold climate conditions. Our work reveals patterns of change within the cyst record reflecting changes in the NAO rather than with any simple abiotic parameter. For the former this may be the result of increased nutrient availability from depth as a result of increased frequencies of upwelling or it might showcase the R-tolerance of the species and hence be able to thrive in waters subjected to increased overturn, upwelling as a result of a particular NAO regime; it is also likely to be a K strategist. It is suspected that the former is also Rtolerant but also an r strategist more amenable to the unpredictable and instability of the spring environment closely following on from the equinoxal storms. It is clearly a complex situation and one that can be argued from several different viewpoints. This study demonstrates the complexity and seeks to avoid a simplistic abiotic interpretation but rather looks to rather larger scale changes within the hydrographic regime reacting to change within the climate patterns within the North Atlantic. To explore some of these ideas further and to look in more detail at other dinoflagellate cysts within our records is outside the scope of this contribution but will ultimately provide a clearer interpretation of the changing marine environment at the annual to decadal scale, a temporal scale so important for predicting our futures.
7. Conclusions This detailed study of the dinoflagellate cyst record of a high resolution sediment record from Gullmar Fjord on the west coast of Sweden has led to some surprises. Contrary to received wisdom the cyst record shows little correlation with the putative ongoing eutrophication in the fjord, and along the west coast of Sweden. Indeed the record of Lingulodinium polyedrum, a suggested index species for eutrophication does not show an ongoing increase in numbers but rather shows a marked decrease since 1970. Its presence within the dinofla-
gellate cyst record is most marked from about 1929 until 1970 having little correlation with the many abiotic instrumental data available from this well studied area and also the known local pollution history. We, therefore, cannot confirm an ongoing eutrophication problem for Gullmar Fjord using the dinoflagellate cyst record nor can we endorse the use of Lingulodinium polyedrum as an eutrophication indicator. In contrast there is a clear change in the dinoflagellate cyst populations at around 1970, as detailed in both spring and late summer cyst producers, which is clearly indicative of a major change in the environment. The only change noted in our study is that accompanying the changeover from a largely negative to positive NAO at about the same time by a decrease in the frequency of upwelling events in the offshore Skagerrak area. The response of the dinoflagellate populations to this change is not easily explained as it is likely to be complex and dynamic. Some attempt has been made to examine these results in the light of a recently published ecological paradigm but a definitive conclusion is not possible at the moment. However we advise against a simplistic interpretation and trust that further work on the ecology of the cyst-forming dinoflagellates might clarify the situation further.
8. Systematic section This section lists the dinoflagellate cysts recovered in Core GA113-2Ab, Gullmar Fjord, Sweden. Taxonomic references can be found in Fensome et al. (1993) for the most part but otherwise are provided herein. Illustrations of many of the relevant dinoflagellate cyst taxa recovered in our study can be found in Rochon et al. (1999) and Harland et al. (2004b), from comparable material in the general North Atlantic area and along the west coast of Sweden. It is beyond the scope of this contribution to provide a fully comprehensive and detailed taxonomic study but the material is available at the University of Go¨teborg. Division DINOFLAGELLATA (Bqtschli, 1885) Fensome et al., 1993. Class DINOPHYCEAE Pascher, 1914. Order GONYAULACALES Taylor, 1980. Family GONYAULACACEAE Lindemann, 1928.
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Genus Ataxiodinium Reid, 1974. Ataxiodinium choane Reid, 1974. Genus Bitectatodinium Wilson, 1973. Bitectatodinium tepikiense Wilson, 1973. Genus Lingulodinium Wall, 1967 emend. Dodge, 1989. Lingulodinium polyedrum (Stein, 1883) Dodge, 1989. Genus Nematosphaeropsis Deflandre et Cookson, 1955 emend. Wrenn, 1988. Nematosphaeropsis labyrinthus (Ostenfeld, 1903) Reid, 1974. Genus Protoceratium Bergh, 1882. Protoceratium reticulatum (Clapare`de et Lachmann, 1859) Bqtschli, 1885. Genus Spiniferites Mantell, 1850 emend. Sarjeant, 1970. Spiniferites bentorii (Rossignol, 1964) Wall et Dale, 1970. Spiniferites delicatus Reid, 1974. Spiniferites elongatus Reid, 1974. Spiniferites lazus Reid, 1974 Spiniferites mirabilis (Rossignol, 1964) Sarjeant, 1970 Spiniferites ramosus (Ehrenberg, 1838) Mantell, 1854. Spiniferites spp. indet. Order PERIDINIALES Haeckel, 1894. Family PERIDINIACEAE Ehrenberg, 1831. Genus Pentapharsodinium Indelicato et Loeblich III, 1986. ?Pentapharsodinium dalei Indelicato et Loeblich III, 1986. Family PROTOPERIDINIACEAE Bujak et Davies, 1998. Genus Islandinium Head et al., 2001. Islandinium cf. cesare (de Vernal et al., 1989 ex de Vernal in Rochon et al., 1999) Head et al., 2001. Genus Lejeunecysta Artzner et Do¨rho¨fer, 1978 emend. Lentin et Williams, 1976. Lejeunecysta marieae (Harland in Harland et al., 1991) Lentin et Williams, 1993. Lejeunecysta oliva (Reid, 1977) Turon et Londeix, 1988. Genus Protoperidinium Bergh, 1881. Protoperidinium avellana (Meunier, 1919) Balech, 1974.
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Protoperidinium claudicans (Paulsen, 1907) Balech, 1974. Protoperidinium compressum (Abe´, 1927) Balech, 1974. Protoperidinium conicoides (Paulsen, 1905) Balech, 1974. Protoperidinium conicum (Gran, 1900) Balech, 1974. Protoperidinium divaricatum (Meunier, 1919) Parke et Dodge, 1976. Protoperidinium leonis (Pavillard, 1916) Balech, 1974. Protoperidinium oblongum (Aurivillius, 1898) Balech, 1974. Protoperidinium pentagonum (Gran, 1902) Balech, 1974. Protoperidinium punctulatum (Paulsen, 1907) Balech, 1974. Protoperidinium subinerme (Paulsen, 1904) Loeblich, 1969. Protoperidinium spp. indet. [peridinioid]. Protoperidinium spp. indet. [round, brown]. Protoperidinium spp. indet. [short spines]. Order GYMNODINIALES Apstein 1909. Family POLYKRIKACEAE Kofoid et Swezy 1921. Genus Gymnodinium von Stein, 1878. Gymnodinium catenatum Graham 1943. Genus Polykrikos Bu¨tschli, 1873. Polykrikos schwartzii Bqtschli 1873. Family UNCERTAIN. Cyst nov. [sparse, spiny].
Acknowledgements The authors would like to thank the crew of the RV Arne Tiselius and RV Skagerak for their assistance in collecting the cores and Mr Steve Ellin and Ahwad B Ibrahim for their technical expertise in processing the samples in the laboratories of the Palynology Research Facility, University of Sheffield. The study was financed by the Swedish Natural Science Research Council (NFR, grants no. G-AA/GU 09874-307 and G-AA/GU 09874-309, K. Nordberg), the Futura Foundation, the Oscar and Lili Lamm Foundation, the Carl Trygger Foundation, the
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