Changes in the diatom community, including the appearance of Actinocyclus normanii f. subsalsa, during the biomanipulation of Lake Vesijärvi, Finland

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1 European Journal of Phycology ISSN: (Print) (Online) Journal homepage: Changes in the diatom community, including the appearance of Actinocyclus normanii f. subsalsa, during the biomanipulation of Lake Vesijärvi, Finland Mikko Liukkonen, Timo Kairesalo & Elizabeth Haworth To cite this article: Mikko Liukkonen, Timo Kairesalo & Elizabeth Haworth (1997) Changes in the diatom community, including the appearance of Actinocyclus normanii f. subsalsa, during the biomanipulation of Lake Vesijärvi, Finland, European Journal of Phycology, 32:4, , DOI: / To link to this article: Published online: 03 Jun Submit your article to this journal Article views: 126 View related articles Citing articles: 10 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 17 September 2016, At: 08:35

2 Eur. J. Phycol. (1997), 32: Printed in the United Kingdom 353 Changes in the diatom community, including the appearance of Actinocyclus normanii f. subsalsa, during the biomanipulation of Lake Vesija rvi, Finland MIKKO LIUKKONEN 1, TIMO KAIRESALO 2 AND ELIZABETH Y. HAWORTH 3 Department of Applied Chemistry and Microbiology, University of Helsinki P.O. Box 56, Helsinki University, FIN Helsinki, Finland Department of Ecological and Environmental Sciences, University of Helsinki, Niemenkatu 73, FIN Lahti, Finland Institute of Freshwater Ecology, Ambleside, Cumbria LA22 0LP, UK (Received 21 November 1996; accepted 25 June 1997) After 60 years of receiving treated sewage effluent from the city of Lahti, Lake Vesija rvi had become very eutrophic. Diversion of the effluent in 1976 resulted in a slow recovery of the water quality. In , biomanipulation removed 380 kg of coarse fish per hectare from Enonselka, the most polluted basin of the lake. Since then cyanobacterial blooms have decreased and water transparency has increased. Paleolimnological analysis of deep water sediments was used to reconstruct the changes in the diatom community, with varved sediment structure providing a year-by-year chronology. During the biomanipulation period the following diatom species increased in Enonselka : Asterionella formosa, Fragilaria crotonensis, Stephanodiscus heterostylus and Tabellaria spp. In contrast, diatom species commonly considered to be indicators of eutrophication, such as Aulacoseira islandica, Diatoma elongatum and Stephanodiscus parvus, have decreased since the end of the 1980s reflecting the recovery of the Enonselka basin. The changes in the diatom plankton recorded in the less polluted basin of Laitialanselka were much less marked than those recorded from the sediments of the Enonselka basin. In 1990 a diatom species, Actinocyclus normanii f. subsalsa, appeared for the first time in Lake Vesija rvi and since then it has been one of the dominant diatoms in the plankton of the Enonselka basin. Two years later it was also present in small numbers in the plankton of Laitialanselka, the least polluted basin of the lake. The appearance of A. normanii f. subsalsa was concomitant with the dredging of the boat harbour of Lahti city in the late summer of It was therefore apparently not directly affected by biomanipulation but benefited indirectly from the collapse of cyanobacterial populations that led to improved light and nutrient availability in the water column. Key words: Actinocyclus, biomanipulation, diatoms, eutrophication, paleolimnology, varved sediment. Introduction As a consequence of sewage discharge from the city of Lahti over a period of some 60 years, Lake Vesija rvi became very eutrophic in the 1960s and 1970s. The discharge was diverted in 1976 but the recovery of the nearby Enonselka basin has been slow due to the high internal nutrient loading (Keto & Sammalkorpi, 1988; Liukkonen et al., 1993). The oxygen concentration of the Enonselka basin in was altered by aeration of the hypolimnion leading to disturbance of the sedimentation process in the deep part of that lake basin during this 6-year period (Liukkonen et al., 1993). Biomanipulation, i.e. the removal of coarse fish (especially roach, Rutilus rutilus L.) by trawling, began in 1989 and, between 1989 and 1993, 980 metric tonnes of fish (380 kg of fish per hectare) were removed from the Enonselka basin. Subsequently cyanobacterial populations have been much reduced and water transparency in the lake basin has increased from m in 1989 to m in 1994 (Kairesalo et al., 1997). Correspondence to: T. Kairesalo. kairesalo neopoli.lpt.fi. Lake Vesija rvi is situated in South Finland between the Salpausselka eskers. It is connected to Lake Pa ija nne by the Va a ksy canal (Fig. 1), which was built in , near the natural outflow. Lake Vesija rvi has four basins (Fig. 1). This study compares sediment samples from the southern, Enonselka basin, the most eutrophic basin of the lake, with those of the western, Laitialanselka basin where the influence of Lahti sewage waters has been least (Table 1). The purpose of this paleolimnological study was to analyse the concomitant changes in the diatom community as accumulated in the deeper water sediments, following methods used earlier (Liukkonen et al., 1993) for the period preceding the biomanipulation. Materials and methods The frozen finger sediment samples were taken in March 1994 through the ice cover from the deepest points of the Enonselka and Laitialanselka basins, using the methods described in Liukkonen et al. (1993). The uppermost 30 cm of the Enonselka sediment and the uppermost 15 cm of the Laitialanselka sediment were analysed. The sedimentation rate was quantified from varve counting. After storing the

3 M. Liukkonen et al. 354 used in phosphorus analyses are described in Liukkonen et al. (1993). Results Fig. 1. A map of Lake Vesija rvi, showing the lake basins, deep areas (shaded) and sampling points (black stars). The location of the natural outlet of the lake (arrow) by the Va a sky canal and the boat harbour (open circle) of the city of Lahti are indicated. Table 1. Hydrological properties of Lake Vesija rvi, the Enonselka basin and the Laitialanselka basin Whole lake Enonselka basin Laitialanselka basin Drainage area (km ) Surface area (km ) Volume (10 m ) Max. depth (m) Mean depth (m) Retention time (years) frozen samples uncovered for some weeks in a freezer ( 20 C), the varves and especially a thick clay layer between 12.0 and 13.5 cm (Fig. 2), became clearly visible. A detailed seasonal diatom succession is based on counts from tape-peel slides following the procedures of Simola (1977). In order to relate the pattern of diatom accumulation more closely to plankton productivity, the counts of the more common taxa have been weighted to provide an estimated percentage of the total biomass, using a volume:weight ratio of approximately 1 g ml. The annual diatom biomass in the Enonselka basin was calculated from the absolute diatom counts according to the methods described in Liukkonen et al. (1993). Scanning electron micrograph preparations were made from cleaned or uncleaned sediment material. The diatom suspensions were dried onto aluminium stubs and coated with platinum in a JEOL Fine Coat JFC-1100 sputtering device. The scanning electron micrographs were then taken using a Zeiss Digital Scanning Microscope 962. The methods Sedimentation rate The varves were proven to be annually laminated from the tape-peel countings, with high valve densities of the dominant diatom species seen at the beginning of the growing season (Fig. 2). The lower part of these analysed sediment samples overlapped with the upper part of the samples of Liukkonen et al. (1993), thus providing comparable diatom and chemical analyses for the period of (Figs 2 6). During the biomanipulation period of , a layer of new sediment 23 cm thick was deposited in the Enonselka deep whereas only 9.5 cm accumulated in the Laitialanselka deep. Varve thickness varied between 3 and 4 cm in the Enonselka sediment, although the uppermost varve and the clay-rich varve of 1990 were thicker. Due to the dredging of the city boat harbour, a substantial amount of clay added a cm thick layer to the sediment of the Enonselka deep in the winter of ; this is represented by the sharp peak in the dry matter and decrease in organic matter (Fig. 3a). After the dredging, clay suspended in the water was distributed by water currents all around the basin in autumn Under ice during the winter, however, the clay accumulated on bottom areas deeper than 20 m. According to the water and bottom samples collected in April 1991 (about 6 months after the dredging), the sedimentation of the finest clay particles was still continuing in the deepest areas of the basin. In the Laitialanselka deep, the sedimentation rate ranged between 1 and 2 cm yr and there were no temporary increases in the sedimentation rate in this basin (Fig. 3 b). Net sedimentation of phosphorus With the exception of the clay layer and superficial loose sediment, average phosphorus concentration, expressed on a dry weight (DW) basis, has ranged between 2 and 3.5 mg P (g DW) in the 1990s (Fig. 3a). According to Liukkonen et al. (1993), it was highest in the Enonselka basin in the early 1970s, being 6 8 mg P (g DW). In the Laitialanselka sediment, phosphorus concentration was highest in the late 1980s, at a little above 2 mg P (g DW), whereafter it has not changed (Fig. 3b). Phosphorus concentration in the surface water in May, during vernal overturn, and the annual net sedimentation of phosphorus in the Enonselka deep, follow the same general declining pattern (Fig. 4). Since the peak years of there have been wide year-to-year fluctuations in the sedimentary accumulation rate, due to differences in oxygen-mediated sorption desorption reactions between phosphorus and iron (cf. Hartikainen et al., 1996). There have also been man-induced perturbations such as dredging and aeration.

4 Paleolimnology of Lake Vesija rvi 355 Fig. 2. Diatom succession in the Enonselka sediment during the years from tape-peel counts. Year labels indicate the spring diatom maxima. (a) Enonselkä (b) Laitialanselkä Fig. 3. Profiles of dry weight (% of fresh weight), loss of ignition (% of dry weight) and phosphorus concentration (mg P g DW) in the Enonselka sediment (a) and Laitialanselka sediment (b). Note differences in scales of the y-axes. Year labels indicate winter time before the start of the growing season.

5 M. Liukkonen et al. 356 Mayer (Figs 12, 13), Tabellaria spp. (T. fenestrata (Lyngbye) Ku tzing and T. flocculosa (Roth) Ku tzing) and Actinocyclus normanii f. subsalsa (Juhlin-Dannfelt) Hustedt (Fig. 5). Examination by scanning electron microscopy suggested that the majority of valves of the larger Stephanodiscus ( 20 µm in diameter) were apparently S. heterostylus. The biomass of one of the dominant vernal diatoms, Aulacoseira islandica (O. Mu ller) Simonsen (Figs 14, 15), has declined since , when it comprised over 40% of the diatom biomass accumulation (Fig. 5). Undoubtedly, the most interesting recent change in the diatom flora is the appearance of Actinocyclus normanii f. subsalsa (Figs 16 18) in the plankton of Enonselka since the beginning of 1990 and, 2 years later, in the plankton of Laitialanselka. Actinocyclus cell numbers have not been very high but, because of its large cell size, this diatom has become a major element in the diatom biomass of Enonselka during the 1990s (Fig. 5). In the Laitialanselka basin, the changes in the percentage biomass shares of different diatoms between 1989 and 1993 have been, as expected, less obvious than those in the Enonselka assemblage (Fig. 6). Fig. 4. Phosphorus concentration (µg Pl ) in the top 5 m of the Enonselka basin in May, between 1970 and 1993, and the accumulation rate of phosphorus in the sediment (g P m yr ) in the deepest part of the basin between 1958 and Changes in the diatom flora since 1989 Small Stephanodiscus cells (5 7 µm in diameter) became very abundant prior to the 1960s (Liukkonen et al., 1993). In the 1990s they were still the most numerous taxa for a short period at the beginning of the spring diatom maximum in Enonselka. However, their contribution to overall diatom biomass has declined since the most eutrophic period of the basin in the 1970s (Fig. 5) and, in the years , the average annual percentages of these forms declined to roughly half of those in the 1970s (Fig. 5). These taxa have been identified as Stephanodiscus parvus Stoermer & Ha kansson and S. rugosus Sieminska & Chudybova, although the latter may be considered as teratological forms of the former (cf. Yang & Duthie, 1993). Scanning electron micrographs clearly show that the identical internal valve structure of S. parvus and S. rugosus (Figs 7 9) includes areolae that are arranged radially, usually in two rows between solid silica interfascicles. There is one rimoportula and one central fultoportula and marginal fultoportulae are at the end of every third or fourth interfascicle. The valve exteriors seem to be heavily silicified (Fig. 8). The diatom species that increased in percentage terms between 1989 and 1993 were Asterionella formosa Hassall, Fragilaria crotonensis Kitton, Stephanodiscus alpinus Hustedt (Figs 10, 11), Stephanodiscus heterostylus Ha kansson & Discussion The summer phosphorus concentration of the water has declined from about 130 µg Pl in the early 1970s to about 30 µg Pl in 1993 in the Enonselka basin (Fig. 4; Kairesalo et al., 1997b). At the same time the annual net sedimentation of total phosphorus has declined from g P m yr to g P m yr in the Enonselka deep (Fig. 4), with the exception of the year 1990, when the dredging of the boat harbour caused a further peak in phosphorus accumulation. The considerable variation in phosphorus accumulation in the sediment in the 1970s is thought to be due to phosphorus release when anaerobic conditions prevail, as happened regularly in the 1970s and 1980s despite the aeration efforts. Hartikainen et al. (1996) concluded that 70 75% of the phosphorus in the Enonselka sediment could be released back to the water under these conditions. On the other hand, the high sedimentation rate of the clay-rich material in may have efficiently prevented the resuspension of phosphorus from the underlying sediment layers. The formation of varved sediment in the deeper parts of the lake basins continued between 1989 and 1993 indicating that, due to high loads of organic matter, anaerobic conditions have continued to develop there, at least temporarily, during periods of stratification. It should, however, be noted that as much as 30 70% of the total sedimentation may have derived from shallow lake areas through resuspension (J. Koski- Va ha la, unpublished data). During , annual sediment accumulation was, on average, about 1 cm higher than that of the preceding 30-year period (Liukkonen et al., 1993). This higher sedimentation rate was not caused by the mass removal of fish but was mainly due to the clay dredged from the boat

6 Paleolimnology of Lake Vesija rvi 357 Fig. 5. Year-to-year diatom accumulation of the 16 main diatom species in Enonselka sediment given as percentage biomass (wet weight % of the most common 20 species). The algal biomass values were determined using a volume:weight ratio of 1 g ml for measured cell volumes. Black bars indicate results from this study; open bars those from Liukkonen et al. (1993). The total biomass (20 planktonic species representing about 95% of all the frustules counted) is based on absolute numbers of the Aulacoseira valves on the microscope slides. Fig. 6. Year-to-year variation in the percentage biomass (wet weight % of the most common 20 species) of 16 diatom species in

7 M. Liukkonen et al. 358 Figs 10, 11. SEM of Stephanodiscus alpinus: outside of the valve. (Scale bars are indicated under the figures.) Figs 7 9. Scanning electron micrographs (SEM) of Stephanodiscus parvus. Fig. 7. S. parvus frustules in uncleaned sediment material. Fig. 8. A frustule from outside. Fig. 9. Inside of a valve. (Scale bars are indicated under the figures.) harbour in This material contained little phosphorus and few diatom valves, as can be seen from the steep decrease in the phosphorus concentration of the sediment of (Fig. 3a) and the absence of diatoms at cm depth (Fig. 2). This layer has provided an excellent marker horizon for the exact dating of the sediment in the diatom analysis. During the biomanipulation period, , the dominant species in the diatom community of the Enonselka basin included more taxa than in the most eutrophic period in the 1970s and 1980s. The dominant species, Aulacoseira islandica, Stephanodiscus alpinus and Stephanodiscus heterostylus, declined between 1989 and 1993, but Asterionella formosa, Fragilaria crotonensis and Tabellaria spp. increased. This reflects the recovery of the basin that was initiated by the diversion of the waste waters of Lahti in 1976 (Liukkonen et al., 1993) and accelerated by the biomanipulation. As small Stephanodiscus spp. are favoured by eutrophic conditions and especially by high phosphorus availability (cf. Stoermer

8 Paleolimnology of Lake Vesija rvi 359 Figs 12, 13. SEM of Stephanodiscus heterostylus: outside of the valve. (Scale bars are indicated under the figures.) et al., 1985; Battarbee, 1986; Anderson, 1989), their decrease, and that of the other eutrophic species, e.g. Aulacoseira islandica and Diatoma tenue var. elongatum Lyngbye, seems to be linked to the reduced phosphorus concentration of the Enonselka water (cf. Kairesalo et al., 1997). Although in both lake basins Aulacoseira islandica seemed to have peaks in abundance at intervals of about 5 or 6 years, with the most striking one being in 1988 (Figs 5, 6), the overall average annual biomass of diatoms has increased between 1989 and 1993 (Fig. 5), suggesting improved growth conditions for diatoms as cyanobacterial populations have declined. With the exception of the new species, Actinocyclus normanii f. subsalsa, the diatom assemblage is reverting to the type that occurred at the end of the 1950s (Liukkonen Figs 14, 15. SEM of Aulacoseira islandica. Fig. 14. Outside of a valve. Fig. 15. Linking spines. (Scale bars are indicated under the figures.) et al., 1993). Actinocyclus normanii f. subsalsa has been found both in eutrophic lakes as well as in brackish water environments (Holland & Claflin, 1975; Stoermer et al., 1992; Ko hler, 1993; van Dam et al., 1994). It is possibly originally a marine or brackish-water species (it was first described from the Baltic coast) that has spread into freshwaters because of eutrophication (Round et al., 1990; Yang et al., 1993) or an increased salinity of the lake water (Hasle, 1977; Gomez, 1991). A. normanii f. subsalsa has been described as a mesothermal (Yang et al., 1993) and alkalibiontic species (with ph optimum above 7 in Husted s ph spectrum). The source of the Actinocyclus normanii f. subsalsa in Enonselka has not been fully identified. Although it appeared in the lake flora at the time of the bio-

9 M. Liukkonen et al. 360 manipulation, it was more closely linked with the dredging of the boat harbour in the autumn of 1990 as the first valves occur just below the clay layer (Fig. 2). During the dredging about m bottom material, i.e. a layer of sediment m thick, was removed from the bottom of the harbour (J. Keto, personal communication). Since A. normanii f. subsalsa is able to rejuvenate from physiologically dormant resting cells (Sicko-Goad et al., 1989), it has possibly come from spores or resting cells released into the water from the dredged sediments. Such rejuvenation has been reported as emanating from 30-yearold sediments in Douglas Lake (Sicko-Goad et al., 1986). However, further study is required to test this and other hypotheses, such as dispersion from the Baltic Sea. To our knowledge, however, A. normanii has not been reported in the plankton of Finnish coastal waters (G. Ha llfors, personal communication) or other Finnish lakes. Diatom taxa that produce resting cells often have seasonal patterns and distributions that differ from other diatoms. Large and heavily silicified species, having relatively high temperature optima, are most abundant in late summer and autumn (Sicko-Goad et al., 1989) and, according to the tape-peel counts, the Actinocyclus maximum in Enonselka occurred later in the summer than those of the other dominant diatom species. Rehbehn et al. (1993) showed that the downstream limit of Actinocyclus normanii f. subsalsa in German North Sea estuaries was mainly determined by light limitation. Biomanipulation thus seems to have had a positive influence on the propagation of Actinocyclus by increasing the transparency in the Enonselka water and favouring this centric diatom during late summer, a period previously dominated by cyanophytes. Acknowledgements The financial support of this study by the Academy of Finland, the Maj and Tor Nessling Foundation and the city of Lahti is greatly appreciated. The scanning electron micrographs were taken at the Institute of Biotechnology, Electron Microscopy, University of Helsinki. We thank Professor Mirja Salkinoja-Salonen for comments on the manuscript, and for support during the completion of the study. References Figs SEM of Actinocyclus normanii f. subsalsa. Fig. 16. Outside of a frustule, Fig. 17. Inside of a valve. Fig. 18. Rimoportula. (Scale bars are indicated under the figures.) ANDERSON, N.J. (1989). A whole-basin diatom accumulation rate for a small eutrophic lake in northern Ireland and its palaeoecological implications. J. Ecol., 77: BATTARBEE, R.W. (1986). The eutrophication of Lough Erne inferred from changes in the diatom assemblages of Pb- and Cs-dated sediment cores. Proc. R. Irish Acad., Section B, 86: GOMEZ, N. (1991). Diatom flora from Embalse Rio III (Prov. Corboda, Argentine). I. Centrales. Gayana Bot., 48 (1 4): 3 9. HARTIKAINEN, H., PITKA NEN, M., KAIRESALO, T.&TUOMINEN, L. (1996). Cooccurrence and potential chemical competition of phosphorus and silicon in lake sediment. Water Res., 30: HASLE, G.R. (1977). Morphology and taxonomy of Actinocyclus normanii f. subsalsa (Bacillariophyceae). Phycologia, 16:

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