A high-resolution dinoflagellate cyst record from latest Holocene sediments in Koljö Fjord, Sweden

Available online at www.sciencedirect.com R

Review of Palaeobotany and Palynology 128 (2004) 119^141 www.elsevier.com/locate/revpalbo

A high-resolution dino£agellate cyst record from latest Holocene sediments in Koljo« Fjord, Sweden Rex Harland a;b; , Kjell Nordberg c , Helena L. Filipsson c b

a DinoData Services, 50 Long Acre, Bingham, Nottingham NG13 8AH, UK Palynology Research Facility, Department of Animal and Plant Sciences, University of She⁄eld, Alfred Denny Building, She⁄eld S10 2TN, UK c Department of Oceanography, Earth Sciences Centre, Go«teborg University, P.O. Box 460, S-40530, Go«teborg, Sweden

Abstract A high-resolution dinoflagellate cyst record is detailed for the very latest Holocene sediments preserved in a silled fjord from western Sweden. Koljo« Fjord is characterised by brackish water conditions together with intermittent deepwater renewal and oxygen depletion. The data provide information derived from the phytoplankton populations living in the surface waters, including possible changes to the nutrient availability and salinity regimes using an actualistic ecological approach. The cyst record provides evidence that the dinoflagellate populations within the surface waters of the fjord over the last 155 years or so have fluctuated markedly. The dinoflagellate cyst record from Core KG1A demonstrates a 10-fold increase in both total cyst numbers and Lingulodinium polyedrum since c. 1938, and a shift from assemblages with high Pentapharsodinium dalei to those with high L. polyedrum and Protoceratium reticulatum from about 1980. These fluctuations are singly and/or collectively indicative of possible cultural changes within the fjord; the effects of the North Atlantic Oscillation on both deep-water renewal and seasonality; nutrient enhancement (eutrophication?); and increased water column stability. 5 2003 Elsevier B.V. All rights reserved. Keywords: dino£agellate cysts; latest Holocene; Koljo« Fjord; palaeoenvironments; hydrography; nutrient availability; eutrophication; salinity; NAO

1. Introduction Koljo« Fjord on the west coast of Sweden is a silled fjord that is characterised by strong water column strati¢cation, stagnant bottom water and periodic periods of hypoxic ( 6 2 ml O2 /l) or anoxic conditions. Occasional renewal of deep water within the fjord occurs during the winter or early spring months when the thermocline is weakest

* Corresponding author. Tel.: +44-1949-875287. E-mail address: [email protected] (R. Harland).

and when there is coastal upwelling of more saline waters in the Skagerrak. At these times the saline coastal waters can cross the sills and £ow into the deeper parts of the fjord, increasing the oxygen content of these deeper waters (Gustafsson and Nordberg, 1999). These conditions are mostly ful¢lled during periods of strong o¡shore northeasterly or easterly winds when surface water is forced o¡shore and Ekman £ow increases the amount of o¡shore upwelling from depth. However, since regular hydrographical measurements of temperature, salinity and oxygen in the fjord began in the early 1950s it has been

0034-6667 / 03 / $ ^ see front matter 5 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0034-6667(03)00116-7

PALBO 2562 20-11-03

120

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

noted that the oxygen de¢ciency of the deep water has occurred periodically, allowing the accumulation of ¢ne clastic laminated sediments. This periodicity in the production of anoxia is also observed in the sedimentary sequence dating from beyond the 1940s and has been the subject of research investigating the nature and cause of this phenomenon during the latest part of the Holocene (Nordberg et al., 2001; Gustafsson and Nordberg, 2002). This study of the dino£agellate cysts is a part of a larger project aimed at understanding the relationship between climate, hydrography and oxygen de¢ciency in bottom sediments from fjords along the west coast of Sweden. The dino£agellate cyst analysis aims to provide a proxy record for environmental conditions primarily in the surface waters of the fjord including climatic variability, nutrient availability and other environmental parameters such as temperature and salinity. It is important in this context to attempt to separate natural variation within the fjord system from cultural factors.

2. Hydrography and circulation Koljo« Fjord is a silled fjord on the west coast of Sweden bordering the Skagerrak. In particular it makes up a part of the open fjord system that surrounds the islands of Tjo«rn and Orust, some 50^100 km north of Go«teborg. The fjord system consists of a number of basins separated by a variety of sills and narrows (Bjo«rk et al., 2000; Nordberg et al., 2001). Koljo« Fjord opens to the Skagerrak to the west across a sill at 8 m depth (S1) via two channel systems, Malo« Stro«mmar and Nordstro«mmarna. To the east it connects to Havstens Fjord across a second sill of 12 m depth (S2) at No«tesund (Fig. 1). Havstens Fjord connects to the Skagerrak to the south over a third sill (S3) of 20 m depth. This sheltered situation ensures that Koljo« Fjord behaves as a basin of net deposition with restricted deep-water access and hence the development of a particularly strong pycnocline. The pycnocline separates the upper, more brackish water (15^27 psu) from the deeper, more saline

waters (27^30 psu) and generally occurs between 15 and 25 m depth within the fjord, but there is also a transitional water layer between 5 and 10 m thick. Koljo« Fjord has a maximum depth of some 56 m. A weak semidiurnal tidal range of 0.15^ 0.2 m amplitude exchanges some surface water between the fjord and the Skagerrak but is of minor importance to the total water exchange within the fjord. Freshwater input into the system derives from the immediate hinterland but is also of minor importance. Water circulation within this fjord system, taken from current measurements (Bjo«rk et al., 2000), indicates an average counterclockwise movement of 100 m3 s31 . More importantly, the fjord is periodically £ushed with saline water from the Skagerrak, via Havstens Fjord to the east, particularly during periods when the prevailing wind is from the north to east, enhancing upwelling in the immediate o¡shore area of the Skagerrak. Further details of the fjord system are available in Bjo«rk et al. (2000) and Nordberg et al. (2001). The basic hydrography of the fjord system on the west coast of Sweden is greatly a¡ected by the in£uence of Baltic waters that lower the salinities of the surface waters of the Kattegat and Skagerrak (Bjo«rk et al., 2000). These lower salinities produce salinity strati¢cation within the fjord system, which because of the sheltered nature of many of the fjords can induce anoxia within the fjord basins, as exempli¢ed within Koljo« Fjord. It has been argued that the production of anoxia may have been worsened by the e¡ects of cultural eutrophication within the area (Nilsson and Rosenberg, 1997); however, decreasing trends in oxygen concentrations within bottom waters over the last 30 years cannot be veri¢ed from the historical dataset from either Koljo« Fjord or nearby Havstens Fjord (Nordberg et al., 2001). In Koljo« Fjord, for most of the time, brackish surface water overlies virtually stagnant saline bottom water that almost inevitably becomes depleted in oxygen from the decay of organic material. Hence the sediments preserved in the fjord are often laminated because of the lack of bioturbation due to the low or nil activity of bottom macrobenthos as oxygen levels fall. These ¢negrained sediments deposited in low oxygen envi-

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

121

Fig. 1. Location map of Koljo« Fjord (A) in relation to the west coast of Sweden (B,C) showing the site of the studied core indicated by the solid black circle. The sill areas are indicated as S1, S2 and S3 (panel B) and isobaths are drawn for the 20 and 40 m depths (panel A). Gbg on the inset map (panel C) refers to the city of Go«teborg and + refers to the monitoring site for the instrumental data.

ronments, often undisturbed by bioturbation and deposited in high accumulation environments, are ideal for the preservation of a high-resolution temporal record that documents change over the recent past within the fjord. Instrumental data collected by the Swedish Meteorological and Hydrological Institute and The Water Quality Association of the Bohus Coast from the surface waters (0^10 m) of Koljo« Fjord are available from the late 1950s to the present time. Several parameters are illustrated in Fig. 2, including salinity; PO4 ; DIN (the sum of NO2 , NO3 and NH4 ); and chlorophyll a, and all of which show little change over time. The salinity was generally slightly higher before 1980 with somewhat higher amplitudes but the other parameters show little change except for the normal annual £uctuations.

Trend analyses, using the Kendell test, on the winter values (Dec., Jan., Feb.) of salinity, PO4 and DIN displayed no signi¢cant trends in the data. However, the winter temperature data for 1958^2000 show a weak signi¢cant rising trend (P 6 0.05) but no signi¢cant trend was found between 1981 and 2000. The summer (Jun., Jul., Aug.) values for all the parameters also displayed no signi¢cant trends (Filipsson and Nordberg, personal communication). The temporal data for chlorophyll a and DIN are, however, relatively short. The phosphate and DIN are a measure of nutrient availability and the chlorophyll a a measure of primary production. The winter nutrient values are more indicative of the size of the available nutrient supply. None of the analysed variables suggests an increased nutrient supply. The winter temperature has increased since the late

PALBO 2562 20-11-03

122

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

Fig. 2. Instrumental data from the surface waters of Koljo« Fjord, including the surface salinity, nutrient content in respect of phosphate and DIN, and primary production as measured by chlorophyll a content.

1950s, probably as a result of the dominance of the positive phase of the North Atlantic Oscillation (NAO) particularly since the 1970s, which has resulted in generally milder winter climates in Scandinavia.

3. Materials and methods Sediment Core KG1A, selected for dino£agellate cyst analysis, was taken in June 1999 using a Gemini corer with an inner core diameter of 80 mm. The core was located (Fig. 1) at latitude 58‡13P62QN, longitude 11‡34P25QE and was taken

at a water depth of 43 m. It was X-rayed onboard ship with an Andrex BV (155 140 kV/5 mA) portable machine before any further investigations took place. In the laboratory the core was sliced and analysed for its organic carbon content (Corg ) using a Carlo Erba NA 1500 instrument. Radiometric dating using the 210 Pb methodology and the constant rate of supply (CRS) model of Appleby and Old¢eld (1978) was carried out at the Department of Radiation Physics, University of Lund, Sweden. Following X-ray analysis the core was sampled for dino£agellate cysts. The results of sediment analysis, organic content and radiometric dating from Koljo« Fjord are pre-

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

sented in Nordberg et al. (2001) and are not repeated herein except where they are relevant to our discussions. Further samples from multicore Core K5B, previously sampled at the same site in September 1998, were processed using simple washing, heavy-liquid separation and ultrasound to assist with the systematics of the recovered cyst species (see Section 7). Samples for dino£agellate cyst analysis were taken at 1- or 2-cm intervals from the ¢negrained, loosely consolidated, organic-rich clastic sediment sequences and processed at the Palynology Research Facility, University of She⁄eld, using the usual palynological processing techniques (see Wood et al., 1996), including a wash with diluted, 6 10%, nitric acid to rid the residues of unwanted amorphous organic material (AOM). Unfortunately, the extremely high content of AOM masked the contained dino£agellate cysts, especially those gonyaulacacean forms that carry spines and processes. The presence of high amounts of AOM can be problematic and it is sometimes di⁄cult to strike an appropriate balance in providing dino£agellate cyst assemblages that can be easily counted without adversely affecting or biasing the proportions of the cysts present. The organic residues were separated from the post acid material using zinc chloride solution with an SG of 1.96 g/cm3 . The resulting organic residue was mounted using Petrapoxy 154 with an RI of 1.54. To enable the calculation of the numbers of cysts per gram of sediment the original dry weight of sediment was noted and aliquots of the organic residues were mounted and counted (Harland, 1989). The organic residues were counted on a single slide either representing 1 g of sediment or a fraction thereof. The cysts per gram data are presented in Table 1; the raw counts data are available from the authors. Dino£agellate cyst spectra were constructed using TILIA/TILIAGRAPH software, and the stratigraphically constrained incremental sum of squares cluster analysis, CONISS (Grimm, 1987), was employed on the cyst/g data to di¡erentiate the various dino£agellate cyst assemblages and to assist in the visual interpretation of the dino£agellate cyst spectra.

123

4. Results Dino£agellate cyst assemblages were recovered from all the samples. It was interesting to note that in Core K5B, samples not processed with acids, dino£agellate cyst cell contents were observed in some specimens to about 30 cm depth, which is equivalent to a date of c. 1920. Dino£agellate cysts together with diatom spores from sediments taken from depth within Koljo« Fjord have been the subject of incubation experiments to ascertain their viability and potential as a seed inoculum (McQuoid et al., 2002). Indeed, the studied assemblage slides produced by this processing technique also yielded excellently preserved, uncompressed cyst specimens, especially those of protoperidiniacean a⁄nity (see Plates I^ III herein) that have informed the systematic part of this study. The dino£agellate cyst spectrum for Core KG1A, Fig. 3, demonstrates a number of features. The ¢rst is that the level of cyst recovery is generally low at less than 500 cysts per gram of sediment below 23.1 cm, whereas above this level the sediment contains cyst numbers often above 2000 cysts per gram. This major division of the cyst assemblages is also re£ected in the stratigraphically constrained cluster analysis that divides Unit II from Unit III herein. The cyst spectrum, together with the stratigraphically constrained cluster analysis, allows the assemblages from Core KG1A to be divided into four informal units characterised by the numbers of cysts per gram of sediment, the nature of the cyst assemblage, including the diversity, and the proportions of the cyst species present. These are described from youngest to oldest below: Unit I, 0.0^9.9 cm, is characterised by reasonably high cyst numbers, often greater than 2000 cysts per gram of sediment, together with a relatively high diversity of 16 species. Important cyst species within this unit include Lingulodinium polyedrum, Protoceratium reticulatum, Spiniferites bentorii, S. elongatus, Protoperidinium conicum (Plate II, 1 and 2), P. oblongum (Plate I, 1 and 2), round, brown Protoperidinium cysts and an informally described species of Protoperidinium

PALBO 2562 20-11-03

124

Table 1 Quantitative data from Koljo« Fjord Core KG1A, including the number of cysts per gram and the total numbers of cysts counted Koljo«fjorden ^ KG1A

PALBO 2562 20-11-03

Gonyaulacacean cysts [A] Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Protoceratium reticulatum Spiniferites belerius Spiniferites bentorii Spiniferites elongatus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet.

0.55

2.75

4.95

7.15

9.35

11.55 13.75 15.95 18.15 20.35 21.45 22.55 23.65 24.75 25.85 26.95 28.05 29.15 30.25 31.35 32.45 33.55 34.65 35.75

/ / 152 130 / 44 / / / 44

/ / 64 137 / 55 9 / / /

/ / 320 448 / 64 13 / / 64

/ / 268 952 / 61 12 / 12 134

/ / 82 222 / 139 / / / 181

/ / 91 103 / 34 / / / 34

/ / 162 149 / 54 41 / / 149

/ / 413 75 / 26 / / / 63

/ / 361 77 / 86 / / / 120

/ / 726 119 / 48 24 / / 83

/ 4 456 180 / 36 12 / / 100

/ / 110 / / 57 5 / 10 14

/ / / 3 / 6 / / / 6

/ / / 4 / 4 / / / 15

/ / 6 3 / / / / / 3

/ / / 5 / 70 3 / / /

/ / / / / 11 / / / /

/ / / / / / 2 / / /

/ / / / / 7 / / / /

/ / / / / 10 / / / /

/ 3 / / / 7 / / / /

/ / 2 / / 46 5 / / /

/ / / 5 / 26 / / / /

/ / / / / 12 2 / / 2

Peridiniacean cysts [A] Pentapharsodinium dalei Congruentidiacean cysts [H] Islandinium minutum Lejeunecysta marieae Lejeunecysta oliva Lejeunecysta paratenella Protoperidinium claudicans Protoperidinium conicum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet.[RB] Protoperidinium sp. A [spinose]

22

/

/

24

/

11

257

100

69

179

264

148

/

/

/

/

/

/

2

/

3

/

/

13

/ / / 22 / 88 22 22 / / / 1367 22

/ / / 46 / 91 9 46 / 9 / 1019 9

/ / / / / 77 / 26 / / / 781 64

/ / / / / 49 / 49 / / / 647 12

/ / / 14 / 28 83 14 / / / 570 42

/ / / / / 34 / 23 / / / 832 57

/ / / / / 95 28 14 / / / 500 /

/ / / / / 138 13 / / / 26 450 13

/ / / / / 275 18 18 / / / 516 9

/ / / 12 / 60 60 95 / / / 809 12

12 / / 4 / 24 / / / / / 128 4

24 / 5 / / / / 10 / / / 171 /

/ / / / / 39 / 3 / / / 100 /

/ / / / / 26 / 4 / / / 111 /

/ / / / / 17 / 6 / / / 195 /

/ / / / 5 3 / 15 / / / 112 /

/ 2 4 / / 5 / 7 / / 2 131 /

/ / / / / 14 / 2 / / / 81 /

/ / / / / / / 11 / / / 11 /

/ / / / / 3 / 15 / / / 10 /

5 / / / / / / 30 / / / 96 /

/ / / / / / / 2 / / / 7 /

2 / / / / 2 / 2 / / / 17 /

/ / / / / / / 3 / / / 13 /

Gymnodinialean cysts Gymnodinium catenatum Polykrikos schwartzii Cyst B of Harland 1977 n

/ 66 / 1996

/ 32 9 1538

/ 13 / 1869

/ 12 37 2269

/ 236 / 2669

/ 57 11 1288

/ 14 / 1458

/ 13 / 1325

/ / / 1548

/ 12 / 2237

/ 4 / 1228

/ / / 552

/ 3 3 161

/ 4 / 167

/ / 3 233

/ 3 3 217

/ 2 / 164

/ / / 100

/ / / 31

/ / / 38

/ 3 / 140

/ 2 / 62

/ / / 55

/ / / 45

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

Depth (cm)

Table 1 (Continued). Depth (cm)

36.85 37.95 39.05 40.15 41.25 42.35 43.45 44.55 45.65 46.75 47.85 48.95 50.05 51.15 52.25 53.35 54.45 55.55 56.65 57.75 58.85 59.95 61.05 62.15

/ / / 5 / 40 3 / / 21

/ / / 2 / 14 5 / / 7

2 / / / / 49 2 / 2 10

/ / 2 9 / 28 7 / / 12

/ / 2 6 / 42 8 / / 20

/ / / / / 27 / / / 13

/ / / / / 55 5 / / 13

/ / 10 19 / 52 / / / 31

/ / 3 19 / 85 / / / 44

/ / 24 / / 170 / / / 61

/ / 5 / / 88 / / / 17

/ / 25 / / 164 / / 6 28

/ / 13 / / 100 / / / 17

/ / 22 / / 198 / / / 34

/ 3 3 / 3 95 / / / 23

/ / 7 / / 83 43 / 17 23

/ / / / / 20 3 / 3 10

/ / / / / 87 / / 2 9

/ / 3 / / 213 / / / 19

/ / 8 / 8 190 / 3 3 30

/ / 10 / / 105 / / / 13

/ / 22 / / 78 / / 6 13

/ / 45 / / 212 / / 6 63

/ / 16 / 2 93 4 / 6 28

Peridiniacean cysts [A] Pentapharsodinium dalei

2

/

40

28

10

5

6

29

27

58

71

78

50

195

160

131

73

62

142

210

151

54

134

71

Congruentidiacean cysts [H] Algidasphaeridium? minutum Lejeunecysta marieae Lejeunecysta oliva Lejeunecysta paratenella Protoperidinium claudicans Protoperidinium conicum Protoperidinium leonis Protoperidinium oblongum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium subinerme Protoperidinium spp. indet. [RB] Protoperidinium sp. A [spinose]

5 / / / / 2 / 3 / / / 69 /

2 / / / / / / 2 / / / 44 /

/ / / / / / / 3 / / / 29 /

/ / / / / / / 5 / / / 37 /

/ / / / / / / 10 2 / / 36 /

/ / / / 2 / / 13 / / / 22 /

/ / / / / / / 21 / / / 19 /

/ / / / / 10 / 31 / / / 155 /

/ / / / / / / 14 / / / 107 /

/ / / / / / / 5 / / / 64 /

/ / / / / 3 / / / / / 10 /

/ / / / / / / / / / / 67 /

/ / / / / / / / / / / 30 /

/ / / / / / / / 3 / / 9 /

/ / / / / / / / / / / 49 /

/ / 3 / / 3 / / / / / 27 /

/ / 3 / / / / / / / / 47 /

/ / / / / 20 / / / / / 47 /

/ / / / / / / 3 / / / 16 /

/ / / / / / / / / / / 30 /

/ / / / / / / / / / / 44 /

/ / / / / / / / 2 / / 16 /

/ / / / / / / / / / / 24 /

2 / 2 / / / / / / / / 12 /

Gymnodinialean cysts Gymnodinium catenatum Polykrikos schwartzii Cyst B of Harland 1977 n

/ / / 150

/ / / 75

/ 2 / 137

/ / / 128

/ 2 / 138

/ / / 81

/ / / 119

/ 12 / 348

/ / / 298

/ / / 382

/ / / 194

/ / / 367

/ / / 210

/ / / 460

/ / / 337

/ / / 336

/ / / 157

/ / / 226

/ / / 396

/ / / 481

3 / / 325

/ / / 189

/ / / 483

/ / / 234

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

PALBO 2562 20-11-03

Gonyaulacacean cysts [A] Ataxiodinium choane Bitectatodinium tepikiense Lingulodinium polyedrum Protoceratium reticulatum Spiniferites belerius Spiniferites bentorii Spiniferites elongatus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. indet.

125

126

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

(Plate III, 3^5) (see Section 7), together with Polykrikos schwartzii. Unit II, 9.9^23.1 cm, contains an assemblage with cyst numbers generally between 1000 and 2000 cysts per gram and a diversity of 14 species. The assemblage is characterised by Lingulodinium polyedrum, Spiniferites bentorii, Pentapharsodinium dalei (Plate II, 4 and 5), Protoperidinium conicum, P. leonis (Plate II, 3; Plate III, 1 and 2), P. oblongum and round, brown Protoperidinium cysts. Unit III, 23.1^44.0 cm, may contain up to 17 species but usually is of low diversity, some nine species, and in contrast to Unit II, described above, has a cyst recovery of only about 150 cysts per gram of sediment. The assemblages are characterised by some Spiniferites species, including S. bentorii and S. elongatus, Protoperidinium oblongum and round, brown Protoperidinium cysts. This unit is notable in lacking the species Lingulodinium polyedrum and Protoceratium reticulatum together with Protoperidinium leonis and the informally described Protoperidinium species (Plate III, 3^5). Unit IV, 44.0^63.25 cm, is a unit of slightly higher diversity of 18 species and cyst numbers that are generally greater than 200 cysts per gram of sediment. This assemblage characteristically contains Spiniferites species, especially S. bentorii and S. ramosus, together with Pentapharsodinium dalei and round, brown Protoperidinium cysts.

5. Discussion First and fundamentally the dino£agellate cyst

127

analysis has revealed signi¢cant £uctuations within the temporal record even over this relatively short time period of about 190 years. This undoubtedly means that the west coast of Sweden, and in particular Koljo« Fjord, has not enjoyed constant environmental conditions but has been subject to change. This is also evidenced by the sediments themselves and in comparison to some of the recorded climatic variables (see Nordberg et al., 2001). It is of particular interest to the scienti¢c community whether these changes are arti¢cial, occurring as the result of some cultural interference within the environment, or whether they are entirely natural and part of the normal pattern of variability. The dino£agellate cyst assemblages are characterised by species of the genera Lingulodinium, Spiniferites and Protoperidinium. Other cyst species such as Nematosphaeropsis labyrinthus and Protoperidinium pentagonum are mostly absent even though they are well known from o¡shore Norway, the North Sea and o¡shore western Scotland (Harland, 1994; Harland and Howe, 1995) and from the most recent sediments in Gullmar Fjord to the north of the present study area (Harland, 2000). Sediment surface samples taken in the Skagerrak and Kattegat (Thorsen et al., 1995; Fjellsafi and Nordberg, 1996) are characterised by Protoceratium reticulatum, Pentapharsodinium dalei, Lingulodinium polyedrum and Spiniferites spp., and by P. reticulatum, L. polyedrum and Spiniferites spp., respectively. The in£uence of the less than fully marine Baltic waters is indicated by the signi¢cant presence of L. polyedrum (Gundersen, 1988). Our assemblages are, therefore, entirely consistent with the locality of Koljo« Fjord and the

Plate I. All the photomicrographs were taken in bright ¢eld and are reproduced at a magni¢cation of U1200. Specimens are identi¢ed by their England Finder coordinates and are ringed. Scale bar is 10 Wm. 1, 2. 1. 2. 3. 4, 5. 4. 5.

Protoperidinium oblongum (Aurivillius, 1898) Balech, 1974. High focus, dorsal view showing the overall morphology and the position of the 2a operculum in place toward the apex of the cyst. Slide RH261A, England Finder N38/2. High focus, ventral view showing the nature of the deeply indented parasulcus. Slide RH260A, England Finder X37/3. Protoperidinium claudicans (Paulsen, 1907) Balech, 1974. Low focus, internal dorsal view showing the operculum in place towards the apex. Slide RH262A, England Finder M27/3. Lejeunecysta marieae (Harland in Harland et al., 1991) Lentin et Williams, 1993. High focus, ventral view showing the parasulcal indentation. Slide RH258A, England Finder M48/0. Low focus showing the overall morphology and the position of the archeopyle. Slide RH258A, England Finder M48/0.

PALBO 2562 20-11-03

128

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

fact that deposition is occurring within a restricted brackish water environment under a tidal in£uence bringing in Baltic waters (Bjo«rk et al., 2000). Three of the main species present, i.e. L. polyedrum, Spiniferites bentorii and Protoperidinium oblongum are also, for instance, well known components of the less than fully marine Irish Sea dino£agellate cyst £ora (see Reid, 1972; Harland, 1977) (see below for further autecological information). A recently published survey of dino£agellate cysts from modern sediments of the west coast of Sweden (Persson et al., 2000) recovered high numbers of L. polyedrum and Pentapharsodinium dalei from Havstens Fjord close to Koljo« Fjord, with the former making up around 50% of the assemblages. A major ¢nding of this research is the 10-fold increase in the numbers of dino£agellate cysts in sediment deposited in the uppermost 23.1 cm part of Core KG1A. Given the 210 Pb chronology the results suggest that this increase in numbers occurs at c. 1938 (Fig. 3). This increase involves the cysts of both heterotrophic and autotrophic dino£agellates and is accompanied by a concomitant marked in£ux of Lingulodinium polyedrum and Pentapharsodinium dalei (Fig. 3) together with Protoceratium reticulatum, Spiniferites spp., Protoperidinium conicum and round, brown Protoperidinium cysts. The signi¢cance of the former two species and especially L. polyedrum is discussed later. This increase in cyst numbers encompasses a time span when measured bottom water salinities plot both above and below a nominal 28.5 psu ¢gure; this empirical ¢gure appears to be signi¢cant for the formation of laminated sediments (see

129

Nordberg et al., 2001); there are both negative and positive NAO Index values ; and both laminated and homogeneous sediments were deposited in the fjord (Nordberg et al., 2001). The dino£agellate cyst content with elevated numbers of Lingulodinium polyedrum together with generally higher numbers of the cysts of heterotrophic dino£agellates can be interpreted as evidence for elevated nutrient values at a time when other measurable factors appear to be quite variable. Indeed, Dale et al. (1999) and Dale and Dale (2002) have identi¢ed the signi¢cant increase in cyst numbers and an increase in numbers of L. polyedrum as a clear eutrophication signal. In our region any increase in the nutrient content of the surface waters of the fjord must derive from the immediate surroundings, including Havstens Fjord, from the rich cocktail of nutrients at depth below the pycnocline or from atmospheric pollution. It should, however, be noted that the measured amounts of phosphate and DIN in the surface waters of the fjord have not signi¢cantly increased since the 1960s and 1980s, respectively (Fig. 2), nor has the general level of primary production since instrumental measurements started in the mid 1980s. However, in addition to the marked increase in the numbers of cysts at c. 1938, there is also a change in the dino£agellate cyst assemblages at around the 9.9 cm depth within the sediments containing the higher cyst numbers. This change in the cyst assemblages is largely characterised by a marked decrease of Pentapharsodinium dalei. This level, dated at 1980, coincides with the changeover from predominantly negative NAO values to the more positive values of the present

Plate II. All the photomicrographs were taken in bright ¢eld and are reproduced at a magni¢cation of U1200. Specimens are identi¢ed by their England Finder coordinates and are ringed. Scale bar is 10 Wm. 1, 2. 1. 2. 3. 4, 5. 4. 5.

Protoperidinium conicum (Gran, 1900) Balech, 1974. High focus, apical view showing the cluster of spines and the symmetrical nature of the mid-dorsal intercalary archeopyle. Slide RH260A, England Finder Q35/0. High focus, dorsal view of the apex showing the symmetrical mid-dorsal archeopyle together with the uncompressed paracingulum. Slide RH260A, England Finder S43/0. Protoperidinium leonis (Pavillard, 1916) Balech, 1974. Low focus, internal dorsal view showing the open mid-dorsal archeopyle and the paracingulum. Slide RH259A, England Finder V32/4. Pentapharsodinium dalei Indelicato et Loeblich III, 1986. High focus, orientation unknown, showing the overall morphology. Slide RH259A, England Finder V42/3. High focus, orientation unknown, showing the overall morphology. Slide RH263A, England Finder X32/0.

PALBO 2562 20-11-03

130

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

day (Fig. 4). Is it possible that the cyst species P. dalei is re£ecting this environmental change in some way? Dale and Fjellsafi (1994) show £uctuations in the numbers of P. dalei (as Peridinium faeroense) in their Oslofjord sediment core that re£ect the Lingulodinium polyedrum curve (as Lingulodinium machaerophorum) and appear, therefore, to be responding as a possible additional eutrophication indicator (see below). However, Dale et al. (1999) admit that little is known of the ecological requirements of P. dalei and that it is not particularly a¡ected by eutrophication. Our results suggest that the scenario is probably more complex and may, in part, re£ect the balance between cyst production of a spring blooming species versus cyst production of a late summer blooming species (see Harland et al., 2004-this issue) linked to the duration of the stability of the water column through the summer and early autumn months. Whilst the dino£agellate cyst evidence appears to suggest strongly that eutrophication has occurred within Koljo« Fjord since 1938, other evidence counters this argument. In particular, the fjord is surrounded by low-lying wooded land, developed on Precambrian and Palaeozoic bedrock. This land is not extensively farmed and provides summer pasture only. Indeed, since the 1950s farming in the area has declined dramatically. In addition, the immediate area has no industry and no large centres of population. It is, therefore, di⁄cult to reconcile the cyst evidence for large-scale eutrophication with the geography of the area, with the lack of increasing measured nutrients within the water column (Fig. 2) and the

131

lack of a marked increase in organic content within the sediments (Fig. 4). The more traditional method of examining the dino£agellate cyst spectrum for environmental information usually involves focussing on ecologically informative species. In this way a more actualistic approach to unravelling the environmental changes occurring within the temporal record should be possible. Species that are important in the dino£agellate cyst spectrum and are rather better known for their autecology are as follows. Lingulodinium polyedrum This dino£agellate species has been associated with localised salinity and temperature regimes, especially lower than normal seawater salinity and large seasonal variation in temperature (Reid, 1972). It has, however, also been associated with higher than normal salinity, with its occurrence in the Straits of Gibraltar (Williams, 1971). Edwards and Andrle (1992) refer to the species as being euryhaline, commonly found in shallow water and having its highest abundance where the sea surface temperature in winter (SSTw ) is s 15‡C, and the sea surface temperature in summer (SSTs ) is s 27‡C. More recently, Rochon et al. (1999) provided optimum SSTw of c. 16‡C, SSTs of c. 22‡C and a sea surface salinity (SSS) of s 36, although they admit that there is evidence for the species occurrence at much lower salinities. Dale and Dale (2002) suggest that this cyst species can only be used as an indication of SSTs of 12‡C or more. Lewis and Hallett (1997), in their very compre-

Plate III. All the photomicrographs were taken in bright ¢eld and are reproduced at a magni¢cation of U1200. Specimens are identi¢ed by their England Finder coordinates and are ringed. Scale bar is 10 Wm. 1, 2. 2. 3. 3^5. 3. 4. 5.

Protoperidinium leonis (Pavillard, 1916) Balech, 1974. Low focus, internal dorsal view showing the position of the mid-dorsal archeopyle together with the paracingulum. Slide RH260A, England Finder K41/0. High focus, ventral view showing the paracingulum and deeply indented parasulcus. Slide RH260A, England Finder K41/0. Protoperidinium sp. A. High focus, orientation unknown, showing the general morphology. Slide RH263A, England Finder L46/0. High focus, orientation unknown, showing the morphology and the dense cover of small aciculate spines together with the excystment aperture, which may be accidental in part but is here regarded as cryptopylic. Slide RH258A, England Finder Q37/4. High focus, orientation unknown, showing the general morphology. Slide RH259A, England Finder V39/3.

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141 Fig. 3. A dino£agellate cyst spectrum of selected species for Core KG1A constructed using the cysts per gram of sediment data. The CONISS cluster analysis together with a visual inspection of the spectrum allows the core to be subdivided into the informal units as shown and discussed in the text. The 210 Pb dating is indicated on the left-hand side of the ¢gure.

132

hensive description of Lingulodinium polyedrum, record that they have grown the species in salinities ranging from 10 to 40 psu. However, they caution against its use as a proxy for salinity alone as reduced salinity enhances water stability; conditions that also favour the growth of L. polyedrum. Also favouring the growth of the species are high nutrient levels (Eppley and Harrison, 1975), leading to the possibility that there is a link between the presence of high numbers of L. polyedrum cysts and high nutrient values. This link between Lingulodinium polyedrum and arti¢cially higher than normal nutrient levels, cultural eutrophication, has been detailed by Madsen and Dale (1992), Dale and Fjellsafi (1994), Thorsen and Dale (1996) and Dale (1998). Indeed, Dale (1996) and Dale and Dale (2002), in their discussion of the utility of using dino£agellate cysts as a signal for eutrophication, suggest that L. polyedrum is a good indicator species for increased nutrient levels and that its presence in low-salinity estuarine environments is a result of high nutrient levels from run-o¡ and not because of ambient low and £uctuating salinities. In addition, Dale (1998) stated that L. polyedrum is a summer blooming species that is able to exploit ‘extra’ nutrients in an otherwise limited nutrient environment. The present work provides, with the recognition of Units I and II in Core KG1A, evidence for a possible eutrophication signal in Koljo« Fjord since 1938 based upon this earlier published research. Indeed, Persson et al. (2000) recognised the high abundances of this species along the west coast of Sweden and explained its presence as evidence for cultural eutrophication. However, the occurrence of the species in nutrient-deplete summer waters (Harland et al., 2004-this issue) lends some support to the evidence from MacIsaac (1978) that Lingulodinium polyedrum migrates vertically through the water column to pick up nutrients from below a nutricline, which in Koljo« Fjord would also coincide with the pycnocline separating the nutrient-poor brackish waters from nutrient-replete saline waters below. Hence in this study the high occurrence of L. polyedrum along this part of the Swedish coast may have nothing to do with cultural eutrophication but may re£ect the hydrography

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

133

Fig. 4. The winter (Jan., Feb., Mar.) NAO index and the Corg from Core K6A plotted against the chronostratigraphy and occurrence of Lingulodinium polyedrum and Pentapharsodinium dalei from Core KG1A. Both cores were collected at the same site and can be closely correlated (Nordberg et al., 2001).

of the fjord systems and the availability of nutrients at depth. Spiniferites bentorii Unfortunately, the cyst species Spiniferites bentorii is not so well provided with autecological information as Lingulodinium polyedrum. The species was ¢rst recognised from the eastern Mediterranean, o¡ the coast of Israel, in both modern and Pleistocene sediments (Rossignol, 1964). Reid (1972) then recorded its presence around the coast of the British Isles and noted its occurrence on

both the west coast of Ireland and on the west coast of Britain with a centre of distribution in Cardigan Bay. He surmised that the species required quite localised seasonal temperature and salinity conditions within semi-enclosed coastal bays. Unfortunately, later studies have not added to these data in any substantial way. The present record of S. bentorii from the Koljo« Fjord core is suggestive that rather localised conditions are required, possibly involving changes in salinity and competition within the dino£agellate £oras; S. bentorii appears to occur in higher numbers

PALBO 2562 20-11-03

134

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

in the earliest part of the sequence in the absence of L. polyedrum and in the presence of Pentapharsodinium dalei. Spiniferites bentorii was recorded, as Gonyaulax digitale, from recent sediments along the west coast of Sweden, especially at Fa«rlevs Fjord, by Persson et al. (2000). Pentapharsodinium dalei This species, not often recorded in the literature, is now being recognised on a more regular basis. It is a small cyst that bears a cover of processes/ spines not unlike those seen on Protoceratium reticulatum. However, the spines are much shorter, delicate and may be branched (see Section 7). The cyst, known under a variety of names, has been recorded from Trondheimsfjord, Norway as ?Scripsiella and generally in the fjords and embayments on both the eastern and western seaboards of the North Atlantic (Dale, 1976, 1977), X byfjorden on the west coast of Sweden including A and from all the sites documented by Persson et al. (2000). It has been referred to as a polar/subpolar species (Dale, 1996), and as a widespread cyst distributed to the north of the main axis of the North Atlantic Current, in southern Hudson Bay and in the eastern Barents Sea (Rochon et al., 1999). Rochon et al. (1999) regarded the species as requiring a minimum SSTs of 4‡C and tending to high relative abundances in areas with large seasonal temperature gradients. The presence of this cyst species is, therefore, di⁄cult to interpret, notwithstanding possible identi¢cation problems (see Section 7), but may be a good indicator of colder temperatures (Dale, 1996). It is also interesting to note that although it may be common in cyst assemblages it has rarely been observed in plankton surveys (Persson et al., 2000). It is perhaps important to our later discussions to note that Dale (1977) found it as a regular component of the spring plankton in Oslofjord and that Harland et al. (2004-this issue) found it as a regular member of the spring (June) phytoplankton bloom in Koljo« Fjord. It is also suggested that there may be some link with negative NAO conditions, colder winters and the preservation and production of laminated sediments within the fjord, as there appears to be some correlation between its high numbers and the presence of lam-

inae in the Koljo« Fjord sedimentary sequence (see below). The dino£agellate cyst record, as discussed herein, has provided information about conditions in the surface waters of the fjord, since neither undue oxidation nor transport have a¡ected the sediments deposited within the fjord basin. The presence of a marked pycnocline also serves to decouple and largely isolate the surface environment from bottom waters. Undoubtedly the dino£agellate cyst record reveals a signi¢cant environmental change post-1938, when cyst numbers and species diversity increased markedly. This may result from eutrophication within the local fjord system or indeed re£ects changes that were occurring on a more regional scale ; it is commonly thought that eutrophication from run-o¡ from farming areas and cities has a¡ected coastal waters along the Swedish west coast (Rosenberg et al., 1996). Although this is true for the southern Kattegat it is not so for this area where farming has been declining since 1960 and there are stringent regulations in place to limit the amount of PO4 and DIN entering the fjord system following sewage treatment. It would appear, therefore, that although the cyst record provides evidence for eutrophication, as discussed above, there is little corroborative evidence. Is there another explanation for the dino£agellate cyst record that does not involve eutrophication ? Other shifts within the cyst assemblages, especially around the 9.9 cm level, also appear to correlate with a change in the NAO from negative to positive values (Fig. 4) and with changes in the salinity regime of the bottom waters, especially since 1980 when the bottom salinity values declined (Nordberg et al., 2001). This apparent correlation between the cyst assemblages and the historical data allows us to recognise a series of possible but tentative scenarios that are described below from the youngest to oldest that do not necessarily involve the process of eutrophication. The ¢rst, operating since 1980, is typi¢ed by Unit I in Core KG1A, and the signi¢cant numbers of Lingulodinium polyedrum, Protoceratium reticulatum, Spiniferites elongatus, Protoperidinium conicum, P. leonis, P. oblongum and Protoperidi-

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

nium sp. nov. This environment is associated with low but variable measured bottom water salinity, higher Corg together with a positive NAO (Nordberg et al., 2001). The positive NAO gives rise to predominantly west to southwesterly prevailing winds, less coastal upwelling leading to generally lower salinities and thereby increasing the frequencies of overturn events, a relatively weaker pycnocline and hence mostly homogeneous sediment deposition within Koljo« Fjord. The dino£agellate cyst assemblage provides evidence for an increased nutrient supply and, in the increased amounts of L. polyedrum, a eutrophication signal following the usual interpretation (Dale et al., 1999; Dale and Dale, 2002). However, the presence of a weak pycnocline allows the di¡usion of oxygen and nutrients to the surface waters from the underlying waters, especially to a dino£agellate species capable of vertical migration to acquire nutrients from below the nutricline (MacIsaac, 1978), in spite of the fact that the measured amounts of phosphate and DIN in the surface waters show little change (Fig. 2). Although bottom water renewal events would provide an enhanced nutrient supply within these bottom waters they seldom take place during the summer. However, any supply across a weaker pycnocline would be su⁄cient to provide Lingulodinium polyedrum with its ‘extra’ nutrients enabling this late summer species to £ourish in the stable and strati¢ed water column along with other species within the £ora. Indeed, data from the phytoplankton blooms sampled in April and June (Harland et al., 2004-this issue) reveal a predominance of Protoperidinium cysts and Pentapharsodinium dalei, respectively, with little evidence of Lingulodinium polyedrum until the late summer bloom sampled in September. Unit II of Core KG1A typi¢es the second, which appears to have operated between 1938 and 1980. Here we have signi¢cant numbers of Spiniferites bentorii and Pentapharsodinium dalei together with Lingulodinium polyedrum. This part of the sedimentary sequence is characterised by laminated sediment, higher measured bottom water salinity and a mostly negative NAO with relatively low Corg (Nordberg et al., 2001). The negative NAO gave rise to frequently occurring

135

easterly and northeasterly winds, with cold, dry winters and often the presence of winter sea-ice cover within the fjord together with increasing o¡shore upwelling. The increase in bottom water salinity resulting from the coastal upwelling prevents or lessens the frequency of deep-water renewals and overturn within the fjord such that there is little supply to enhance the nutrient content within the surface waters. These waters are relatively una¡ected by changes below a strong pycnocline, which prevents the di¡usion of oxygen and nutrients. E¡ectively the surface waters may be nutrient-deplete and isolated from the deep-water source but contain su⁄ciently high nutrient content in the spring from local run-o¡ to favour the spring phytoplankton bloom over the late summer bloom; this leads to an increase in P. dalei rather than L. polyedrum. The presence of cryophilic P. dalei (Dale, 1996) is also evidence of colder winter climates at this time. It is of interest to note that major engineering works were carried out to the fjord between 1936 and 1946 to deepen the western sill to make it easier for large ships to reach Uddevalla. In addition, between 1939 and 1943 the Bjo«rnsund channel at Malo« Stro«mmar was also built. It is a worthy speculation that these engineering works may also have had an e¡ect on the phytoplankton populations within the fjord, allowing for the inoculation of the fjord with species more commonly associated with the Skagerrak. Unit III in Core KG1A, encompassing the years 1850^1938, consists of a homogeneous sediment record under a predominantly positive NAO regime (Nordberg et al., 2001). Unfortunately, the salinity record is not known in detail but it is assumed that bottom water salinities are again lower, with a greater frequency of overturn events. The dino£agellate cyst record is poor but contains Spiniferites bentorii, S. elongatus and Protoperidinium oblongum and a distinct lack of Lingulodinium polyedrum. However, the low numbers of cysts and the relatively low Corg (Nordberg et al., 2001) are evidence of lower nutrient values in the surface waters due to little recharge of nutrients from bottom waters and little input from the immediate hinterland. In Unit IV there is a slight increase in cyst

PALBO 2562 20-11-03

136

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

numbers accompanied by the presence of Spiniferites bentorii and Pentapharsodinium dalei. However, the cyst assemblage, if not indicative of higher nutrient availability, i.e. lack of Lingulodinium polyedrum and the cysts of heterotrophic dino£agellates, could be reacting to a di¡erent salinity regime and be indicative of more negative NAO values with increased o¡shore upwelling and decreasing deep-water renewal within the fjord system. The presence of P. dalei may be indicative of the importance of the spring phytoplankton bloom at the expense of the late summer bloom of L. polyedrum rather than an indicator of colder winters. More saline and/or colder bottom water conditions are also suggested by the oxygen isotope data from the benthic foraminifera (Gustafsson and Nordberg, 2002). It is obvious from our discussions that the interpretation of these high-resolution records is dif¢cult, if not virtually impossible, without good syn- and autecological information. We have attempted to examine the dino£agellate cyst record from Koljo« Fjord in relation to the known salinity £uctuations and to the calculated NAO. The cyst record is somewhat isolated or decoupled from the sediment sequence within the fjord (Nordberg et al., 2001), which is more closely related to bottom water environments below the pycnocline rather than to surface environments. However, negative NAO values, higher bottom salinities and an enhanced strati¢cation appear, in this instance, to favour particular increases in the numbers of the dino£agellate cyst species Pentapharsodinium dalei and Spiniferites bentorii. These species are not utilising increased nutrients crossing a strong pycnocline and, in the case of the ¢rst mentioned, are spring bloomers and indicators of cold winters rather than late summer species. This is in contrast to the situation of positive NAO values, lower bottom salinities and a weaker pycnocline that enhances dino£agellate cyst production particularly from the late summer species, especially Lingulodinium polyedrum.

6. Conclusions The high-resolution dino£agellate cyst record

recovered from Koljo« Fjord provides the evidence to outline a number of environmental changes within the very latest part of the Holocene. Indeed the 210 Pb chronostratigraphy suggests that the sediments preserved in the fjord, and studied herein, encompass pre-1855 to the present day. The cyst record not only demonstrates signi¢cant environmental change within the last 150 years or so but also serves as a tool for the subdivision of the sediment sequence. In particular, the dino£agellate cyst record can be interpreted as possible evidence for some nutrient enhancement within Koljo« Fjord. It is, however, somewhat debatable as to the source of the nutrient enhancement since the immediate hinterland of Koljo« Fjord supports no industry, has not witnessed any increased population or increased agriculture. Indeed, there has also been no signi¢cant change in the winter nutrient concentrations within the coastal waters outside the fjord system in the recent past (Andersson, 1996). In summary, this evidence encompasses a 10-fold increase in the cyst content of the sediment and the increased presence of the dino£agellate species Lingulodinium polyedrum. Although often cited as evidence of eutrophication we believe that there could be an alternative explanation in that these signals are linked to the supply or availability of nutrients from depth, which in itself varies according to the nature of the NAO. It will be obvious from our discussions that the most signi¢cant constraint on the interpretation of the cyst record is the lack of autecological and synecological information on the dino£agellate cysts recovered from these fjord sediments. It has been our intention to use such information as and where possible as our principal guide to interpretation. The provision of further and more detailed ecological information can only enhance any technique available to the analyst. It is becoming clear that the changes in the dino£agellate cyst populations occur as a result of many complex interactions that require further study for their elucidation. We are also aware that transfer function techniques are being used by some workers to assist in their interpretations of the recent fossil record (GrYsfjeld et al., 1999; de Vernal et al., 2000).

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

For the moment we prefer to see these high-resolution fjord cyst assemblages, described above, as a very particular series of environments that are not immediately suitable for the transfer function technique at this scale. This technique appears to work rather better at a larger, ocean-wide scale, where it is less constrained by the North Atlantic database from which the best analogue transfer function is derived. Indeed, it is clear from our evidence that the responses of the dino£agellate populations to environmental change, both arti¢cial and natural, are complex and may not be entirely suitable for transfer function techniques until a more suitable database is available based upon the many and varied fjord environments. Indeed, the use of the transfer function technique to relate cyst distributions across ocean basins to surface water parameters and hence to provide quantitative information of past conditions has recently come under some scrutiny and criticism (Dale, 1996; Dale and Dale, 2002). Much of this criticism derives from the fact that dino£agellate cysts have the ability to be transported over large distances outside their normal habitat and, therefore, do not necessarily re£ect the overlying surface water environment, the basic assumption that is the foundation for the use of the transfer function technique. We believe that many of the present di⁄culties and controversies may well have more of a basis within the scale and constraints of the studies being undertaken. For the moment we are content to follow the conservative approach outlined above until further evidence is available.

137

for that of Head et al. (2001), which is listed herein. Division DINOFLAGELLATA (Bu«tschli, 1885) Fensome et al., 1993 Class DINOPHYCEAE Pascher, 1914 Order GONYAULACALES Taylor, 1980 Family GONYAULACACEAE Lindemann, 1928 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 Protoceratium Bergh, 1882 Protoceratium reticulatum (Clapare'de et Lachmann, 1859) Bu«tschli, 1885 Remarks: The authors experienced some di⁄culty in di¡erentiating between small specimens of Protoceratium reticulatum and Pentapharsodinium dalei, see further comments below. These cysts, with cell contents and accumulated organic debris attached to their processes, could often only be identi¢ed with con¢dence from the small cavity at the proximal end of the process that is expressed as a ‘doughnut’-shaped ring in plan view. Some small P. reticulatum cysts may have been included, in part, with the P. dalei count.

7. Systematics All the dino£agellate cysts recovered in Core KG1A, Koljo« Fjord, Sweden, are listed below. Taxonomic comments are reserved for some of the more contentious taxa and one taxon is informally described. The illustrated material and the specimens of the new species are lodged in the collections of the Department of Oceanography, Go«teborg University. Taxonomic references cited here can be found in Williams et al. (1998) except

Genus Spiniferites Mantell, 1850 emend. Sarjeant, 1970 Spiniferites belerius Reid, 1974 Spiniferites bentorii (Rossignol, 1964) Wall et Dale, 1970 Spiniferites elongatus Reid, 1974 Spiniferites frigidus Harland et Reid in Harland et al., 1980 Spiniferites membranaceus (Rossignol, 1964) Sarjeant, 1970

PALBO 2562 20-11-03

138

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

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 (Plate III, 4 and 5) Remarks : This cyst may have been confused in part with small specimens of Protoceratium reticulatum. In part this confusion stems from the fact that this taxon has never been described in the literature in su⁄cient detail to assist in its unequivocal identi¢cation. Dale (1977) described the cysts as being spherical with a variable covering of processes that are solid with distinctive terminations that may be branched but are usually unbranched. The cysts are between 19 and 36 Wm in diameter with processes of between 1 and 8 Wm in length and they appear to open by means of a simple cryptopylic split. More recently, Rochon et al. (1999) have provided a little more detail, including the fact that the cysts are best seen using interference contrast microscopy.

the BGS Ormesby Borehole as Lejeunecysta (Protoperidinium sect. Lejeunecysta) mariea (Harland et al., 1991) is now also known from Late Pliocene St Erth Beds of Cornwall (Head, 1993), the Late Pliocene of the Royal Society Borehole at Ludham, Norfolk (Head, 1996), the Late Pliocene of the Red Crag at Walton-on-the-Naze (Head, 1998) and the latest Pliocene of the Clino Core, Bahamas (Head and Westphal, 1999). It is, perhaps, surprising to identify it here within these very latest Holocene sediments; its occurrence may re£ect particular environmental conditions, as it is unlikely to result from reworking in this sedimentary setting. Lejeunecysta oliva (Reid, 1977) Turon et Londeix, 1988 Genus Protoperidinium Bergh, 1881 Protoperidinium avellana (Meunier, 1919) Balech, 1974 Protoperidinium claudicans (Paulsen, 1907) Balech, 1974 (Plate I, 3) Protoperidinium conicoides (Paulsen, 1905) Balech, 1974 Protoperidinium conicum (Gran, 1900) Balech, 1974 (Plate II, 1 and 2)

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 (Plate I, 4 and 5)

Remarks: This species often occurs uncompressed, even though oriented on the slides in an apical/antapical position. The two specimens illustrated demonstrate this clearly and show the morphology of the paracingulum, the epicyst and the 2a dorsal intercalary archeopyle with the operculum in place (Plate II, 2). We believe, contrary to many descriptions, that the archeopyle is not o¡set, a feature often used to di¡erentiate these cysts, but that it is symmetrical in the mid-dorsal position as with other representatives of the genus. The apparent o¡set position, often reported in the literature, is an artefact of preservation and compression whereby the broad paracingulum folds in such a way as to move the epicyst out of alignment with the hypocyst and hence e¡ectively to o¡set the archeopyle.

Remarks : This cyst, ¢rst described from the Early Pleistocene, now Late Pliocene, Crag deposits of

Protoperidinium compressum (Abe¤, 1927) Balech, 1974

Family PROTOPERIDINIACEAE Bujak et Davies, 1998 Genus Islandinium Head et al., 2001 Islandinium minutum (Harland et Reid in Harland et al., 1980) Head et al., 2001 Islandinium ? var. cesare (de Vernal et al., 1989 ex de Vernal in Rochon et al., 1999) Head et al., 2001

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

Protoperidinium leonis (Pavillard, 1916) Balech, 1974 (Plate II, 3; Plate III, 1 and 2) Protoperidinium oblongum (Aurivillius, 1898) Balech, 1974 (Plate I, 1 and 2) Protoperidinium pentagonum (Gran, 1902) Balech, 1974 Protoperidinium punctulatum (Paulsen, 1907) Balech, 1974 Protoperidinium subinerme (Paulsen, 1904) Loeblich, 1969 Protoperidinium spp. indet. [round, brown cysts] Protoperidinium sp. A [short spines] [H] (Plate III, 3^5) Description: This small brown cyst is spheroidal to ovoidal. The cyst wall appears to be of autophragm alone and is about 0.25 Wm in thickness and smooth. The cyst carries a dense cover of solid spines ; these spines are numerous, about 1.0 Wm in length, subconical to tapering, slender, erect to slightly sinuous with an aciculate distal tip. The spines do not appear to be organised to re£ect a paratabulation. The cyst does not exhibit an unequivocal archeopyle although some specimens show breakage of the wall that appears to be not accidental, nor can it be related to paratabulation; the archeopyle is, therefore, cryptopylic in nature. The cysts are 43^47 Wm in longest dimension and 27^43 Wm in the shortest dimension. Order GYMNODINIALES Apstein, 1909 Family POLYKRIKACEAE Kofoid et Swezy, 1921 Genus Polykrikos Bu«tschli, 1873 Polykrikos schwartzii Bu«tschli, 1873

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, Ahwad B. Ibrahim and Rob Cook for their technical expertise in processing the samples in the laboratories of the Palynology Research Facility, University of She⁄eld. Professor A. Traverse and

139

Dr Niels E. Poulsen are thanked for their constructive criticisms of an earlier version of the manuscript. The study was ¢nanced by the Swedish Natural Science Research Council (NFR, Grants no. G-AA/GU 09874^307 and G-AA/ GU 09874-309, K.N.), the Futura Foundation, the Oscar and Lili Lamm Foundation, the Carl Trygger Foundation, the Wafihlstro«m Foundation and Go«teborg University Marine Research Centre (GMF).

References Andersson, L., 1996. Trends in nutrient and oxygen concentrations in the Skagerrak-Kattegat. J. Sea Res. 35, 63^71. Appleby, P.G., Old¢eld, F., 1978. The calculation of lead-210 dates using a constant rate of supply of unsupported 210Pb to the sediment. Catena 5, 1^8. Bjo«rk, G., Liungman, O., Rydberg, L., 2000. Net circulation and salinity variations in an open-ended Swedish fjord system. Estuaries 23, 367^380. Dale, B., 1976. Cyst formation, sedimentation, and preservation: factors a¡ecting dino£agellate assemblages in Recent sediments from Trondheimsfjord, Norway. Rev. Palaeobot. Palynol. 22, 39^60. Dale, B., 1977. New observations on Peridinium faeroense Paulsen (1905), and classi¢cation of small orthoperidinioid dino£agellates. Br. Phycol. J. 12, 241^253. Dale, B., 1996. Dino£agellate cyst ecology: modelling and geological applications. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications, vol. 3. American Association of Stratigraphic Palynologists Foundation, Dallas, TX, pp. 1249^1275. Dale, B., 1998. Marine dino£agellate cysts as indicators of cultural eutrophication, industrial pollution, and short term climatic change. In: Smelror, M. (Ed.), Abstracts from the Sixth International Conference on Modern and Fossil Dino£agellates, Dino6, Trondheim, Norway, June 1998. NTNU Vitenskapsmuseet, Rapport botanisk serie 1998-1, pp. 27^28. Dale, B., Dale, A.L., 2002. Environmental applications of dino£agellate cysts and acritarchs. In: Haslett, S.K. (Ed.), Quaternary Environmental Micropalaeontology. Arnold, London, pp. 207^240. Dale, B., Fjellsafi, A., 1994. Dino£agellate cysts as paleoproductivity indicators: state of the art, potential and limits. In: Zahn, R., et al. (Eds.), Carbon Cycling in the Glacial Ocean: Constraints on the Ocean’s Role in Global Change. Springer, Berlin, pp. 521^537. Dale, B., Thorsen, T.A., Fjellsafi, A., 1999. Dino£agellate cysts as indicators of cultural eutrophication in the Oslofjord, Norway. Estuar. Coast. Shelf Sci. 48, 371^382. de Vernal, A., Hillaire-Marcel, C., Turon, J.-L., Matthiessen,

PALBO 2562 20-11-03

140

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141

J., 2000. Reconstruction of sea-surface temperature, salinity, and sea-ice cover in the northern North Atlantic during the last glacial maximum based on dinocyst assemblages. Can. J. Earth Sci. 37, 725^750. Edwards, L.E., Andrle, V.A.S., 1992. Distribution of selected dino£agellate cysts in modern marine sediments. In: Head, M.J., Wrenn, J.H. (Eds.), Neogene and Quaternary Dino£agellate Cysts and Acritarchs. American Association of Stratigraphic Palynologists Foundation, Dallas, TX, pp. 259^288. Eppley, R.W., Harrison, W.G., 1975. Physiological ecology of Gonyaulax polyedra a red water dino£agellate of southern California. In: LoCicero, V.R. (Ed.), Proceedings of the First International Conference on Toxic Dino£agellate Blooms, Massachusetts Science and Technology Foundation, Wake¢eld, MA, pp. 11^22. Fjellsafi, A., Nordberg, K., 1996. Toxic dino£agellate ‘blooms’ in the Kattegat, North Sea, during the Holocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 124, 87^105. Grimm, E.C., 1987. CONISS: a FORTRAN 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Comput. Geosci. 13, 13^35. GrYsfjeld, K., Larsen, E., Sejrup, H.P., de Vernal, A., FlatebY, T., VestbY, M., Ha£idason, H., Aarseth, I., 1999. Dino£agellate cysts re£ecting surface-water conditions in Voldafjorden, western Norway during the last 11 300 years. Boreas 28, 403^415. Gundersen, N., 1988. En palynologisk undersYkelse av dino£agellatcyster langs en synkende salinitetsgradient I recente sedimenter fra ^stersjY-omrafidet. Unpublished candidata scientiarum thesis, University of Oslo, pp. 1^96. Gustafsson, M., Nordberg, K., 1999. Benthic foraminifera and their response to hydrography, periodic hypoxic conditions and primary production in the Koljo« fjord on the Swedish west coast. J. Sea Res. 41, 163^178. Gustafsson, M., Nordberg, K., 2002. The impact of climate and shore-level displacement on the late-Holocene environmental development of Havstens Fjord and Koljo« Fjord, Swedish west coast. Holocene 12, 325^338. Harland, R., 1977. Recent and Late Quaternary (Flandrian and Devensian) dino£agellate cysts from marine continental shelf sediments around the British Isles. Palaeontographica B 164, 87^126. Harland, R., 1989. A dino£agellate cyst record for the last 0.7 Ma from the Rockall Plateau, northeast Atlantic Ocean. J. Geol. Soc. London 146, 945^951. Harland, R., 1994. Dino£agellate cysts from the glacial/postglacial transition in the northeast Atlantic Ocean. Palaeontology 37, 263^283. Harland, R., 2000. Dino£agellate cyst analysis of Late Holocene sediments from Core G113-2A, Gullmar Fjord, Sweden. Unpublished DinoData Services Report RH/00/08/01, pp. 1^13. Harland, R., Bonny, A.P., Hughes, M.J., Morigi, A.N., 1991. The Lower Pleistocene stratigraphy of the Ormesby Borehole, Norfolk, England. Geol. Mag. 128, 647^660. Harland, R., Howe, J.A., 1995. Dino£agellate cysts and Ho-

locene oceanography of the northeastern Atlantic Ocean. Holocene 5, 220^228. Harland, R., Nordberg, K., Filipsson, H.L., 2004. The seasonal succession of dino£agellate cysts in Koljo« Fjord, west coast of Sweden. Rev. Palaeobot. Palynol. 128, DOI: 10.1016/S0034-6667(03)00115-5 (this issue). Head, M.J., 1993. Dino£agellates, sporomorphs, and other palynomorphs from the Upper Pliocene St. Erth Beds of Cornwall, southwestern England. Paleontol. Soc. Mem. 31, 1^62. Head, M.J., 1996. Late Cenozoic dino£agellates from the Royal Society borehole at Ludham, Norfolk, eastern England. J. Paleontol. 70, 543^570. Head, M.J., 1998. Pollen and dino£agellates from the Red Crag at Walton-on-the-Naze, Essex: evidence for a mild climatic phase during the early Late Pliocene of eastern England. Geol. Mag. 135, 803^817. Head, M.J., Harland, R., Matthiessen, J., 2001. Cold marine indicators of the late Quaternary: the new dino£agellate cyst genus Islandinium and related morphotypes. J. Quat. Sci. 16, 621^636. Head, M.J., Westphal, H., 1999. Palynology and palaeoenvironments of a Pliocene carbonate platform: the Clino core, Bahamas. J. Paleontol. 73, 1^25. Lewis, J., Hallett, R., 1997. Lingulodinium polyedrum (Gonyaulax polyedra) a blooming dino£agellate. In: Ansell, A.D., Gibson, R.N., Barnes, M. (Eds.), Oceanography and Marine Biology: an Annual Review. UCL Press, London, pp. 97^ 161. MacIsaac, J.J., 1978. Diel cycles of inorganic nitrogen uptake in a natural population dominated by Gonyaulax polyedra. Limnol. Oceanogr. 23, 1^9. Madsen, A., Dale, B., 1992. Dino£agellate cysts as indicators of eutrophication in the inner part of Oslofjord, southern Norway. Program and Abstracts, 8th International Palynological Congress, Aix-en-Provence, France, p. 95. McQuoid, M., Godhe, A., Nordberg, K., 2002. Viability of phytoplankton resting stages in coastal Swedish sediments. Eur. J. Phycol. 37, 191^201. Nilsson, H.C., Rosenberg, R., 1997. Benthic habitat quality assessment of an oxygen stressed fjord by surface and sediment pro¢le images. J. Mar. Syst. 11, 249^264. Nordberg, K., Filipsson, H.L., Gustafsson, M., Harland, R., Roos, P., 2001. Climate, hydrographic variations and marine benthic hypoxia in Koljo« Fjord, Sweden. J. Sea Res. 46, 187^200. Persson, A., Godhe, A., Karlson, B., 2000. Dino£agellate cysts in recent sediments from the west coast of Sweden. Bot. Mar. 43, 69^79. Reid, P.C., 1972. Dino£agellate cyst distribution around the British Isles. J. Mar. Biol. Assoc. UK 52, 939^944. Rochon, A., de Vernal, A., Turon, J.-L., Matthiessen, J., Head, M.J., 1999. Distribution of Recent dino£agellate cysts in surface sediments from the North Atlantic Ocean and adjacent seas in relation to sea-surface parameters. American Association of Stratigraphic Palynologists Foundation, Contribution Series 35, pp. 1^146.

PALBO 2562 20-11-03

R. Harland et al. / Review of Palaeobotany and Palynology 128 (2004) 119^141 Rosenberg, R., Cato, I., Forlin, L., Grip, K., Rodhe, J., 1996. Marine environment quality assessment of the SkagerrakKattegat. J. Sea Res. 35, 1^8. Rossignol, M., 1964. Hystrichosphe'res du Quaternaire en Me¤diterrane¤e orientale, dans les sediments Ple¤istoce'nes et les boues marines actuelles. Rev. Micropale¤ontol. 7, 83^99. Thorsen, T.A., Dale, B., 1996. Dino£agellate cysts as indicators of marine pollution and climatic change in a Norwegian fjord. Ninth International Palynological Congress, Houston, TX, Program and Abstracts, p. 160. Thorsen, T.A., Dale, B., Nordberg, K., 1995. ‘Blooms’ of the toxic dino£agellate Gymnodinium catenatum as evidence of climatic £uctuations in the late Holocene of southwestern Scandinavia. Holocene 5, 435^446.

141

Williams, D.B., 1971. The occurrence of dino£agellates in marine sediments. In: Funnell, B.M., Riedel, W.R. (Eds.), Micropalaeontology of Oceans. Cambridge University Press, Cambridge, pp. 231^243. Williams, G.L., Lentin, J.K., Fensome, R.A., 1998. The Lentin and Williams index of fossil dino£agellates 1998 edition. American Association of Stratigraphic Palynologists, Contribution Series 34, pp. 1^817. Wood, G.D., Gabriel, A.M., Lawson, J.C., 1996. Palynological techniques - processing and microscopy. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications, vol. 1. American Association of Stratigraphic Palynologists Foundation, Dallas, TX, pp. 29^50.

PALBO 2562 20-11-03