HABITAT-INDUCED HETEROGENEITY IN THE CURONIAN LAGOON LITTORAL ASSEMBLAGES: MYSIDS, JUVENILE FISH AND PLANKTON CRUSTACEANS

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1 312 Acta Zoologica Lituanica, 2005, Volumen 15, Numerus 4 ISSN HABITAT-INDUCED HETEROGENEITY IN THE CURONIAN LAGOON LITTORAL ASSEMBLAGES: MYSIDS, JUVENILE FISH AND PLANKTON CRUSTACEANS Jûratë LESUTIENË, Zita Rasuolë GASIÛNAITË, Evelina GRINIENË Coastal Research and Planning Institute, Klaipëda University, Manto 84, LT Klaipëda, Lithuania. kubiliute@corpi.ku.lt Abstract. Zooplankton, juvenile fish and mysid assemblages were investigated in adjacent vegetated and un-vegetated littoral habitats of the Curonian Lagoon (SE Baltic Sea). Juvenile perch (Perca fluviatilis) showed significant habitat partitioning while roach (Rutilus rutilus) did not. The proportion of perch was higher in vegetated habitats, and its foraging on Daphnia was lower in open areas. Roach preferred frequent shifting between habitats, and foraged more intensely on Daphnia and copepods in un-vegetated areas or fed on small-sized chydorids regardless of habitat facilitation. Two omnivorous Ponto-Caspian mysids (Limnomysis benedeni and Paramysis lacustris) tend to aggregate in vegetation during nocturnal migrations. However, their hypothetically increased predatory potential did not show a clear structuring effect on zooplankton distribution in littoral habitats at night. In contrast, the research cases showed that zooplankton distribution heterogeneity is more pronounced during the day. We suggested several specific features of the horizontal distribution of cladocerans during the day in relation to littoral vegetation and fish predation potential. Other important factors such as hydrodynamic should be considered to elaborate the full model of zooplankton horizontal distribution within littoral habitats of the Curonian Lagoon. Key words: submerged macrophytes, zooplanktivory, diurnal changes INTRODUCTION Submerged vegetation is an essential factor in determining the structure of littoral assemblages and affecting food-web interactions in shallow waters (Carpenter & Lodge 1986; Stanfield et al. 1997; Jeppesen et al. 1998; Donk & Bund 2002). This vegetation reduces feeding efficiency of planktivorous juvenile fish by providing spatial refuge for zooplankton (Moss et al. 1998; Bertolo et al. 1999; Burks et al. 2001). On the other hand, juveniles of some fish species have specific adaptations to foraging in vegetated habitats (Persson & Eklöv 1995), therefore the presence of macrophytes can have an adverse effect, leading to a decline of zooplankton in the littoral zone (Nurminen & Horppila 2002). Moreover, the presence of zooplanktivorous invertebrate predators in vegetation or adjacent open areas can lead to an additional structuring effect on zooplankton distribution (Smiley & Tessier 1998) particularly at night when most invertebrate predators are migrating to feed in the upper water layers (Lampert & Sommer 1997). There is still a lack of knowledge of the spatio-temporal zooplankton distribution pattern in vegetated and open habitats of brackish water ecosystems under the combined influence of planktivorous fish and mysids (Jeppesen 1998; Sondergaard et al. 2000). The Curonian Lagoon (the southeastern part of the Baltic Sea) is a brackish water basin with welldeveloped submerged littoral vegetation stocked with planktivorous juvenile fish and omnivorous littoral mysids. The stomach content analysis showed that mysids tend to be predatory only during their nocturnal migrations (Jankauskienë 2000). The general patterns of juvenile fish and mysid spatial distribution in the lagoon are described on the basis of large-scale sampling (Razinkovas 1996; Þiliukienë 1998; Þiliukienë & Þiliukas 2000; Þiliukas 2003), but no attempt was made to evaluate their microhabitat use in vegetated littoral areas. The information on spatio-temporal dynamics of zooplanktivores and zooplankton structure would precise quantitative estimates in vegetated littoral habitats and will be important to better understand the functioning of the littoral plankton food web. Our aim was to delineate habitat preferences of juvenile fish and mysids as well as foraging patterns of juvenile fish in adjacent vegetated versus un-vegetated habitats both during the day and the night. One of the limiting factors in sampling littoral microhabitats is the unsuitability of towed sampling gear, commonly used for fish and mysid research in the lagoon, in vegetation (Rozas & Minello 1997). We selected trapping as a passive sampling method which enabled us to

2 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 313 differentiate habitat boundaries on a fine spatial scale and to collect combined mysid-fish samples at night. Two typical cases of the macrophyte edge were distinguished: the macrophyte edge bordering an open pelagic zone and the edge of a separate macrophyte bed in a patchy extended littoral zone. Habitat-related diurnal changes in the structure of the crustacean zooplankton assemblage were expected. MATERIAL AND METHODS Description of the study site. The Curonian Lagoon (the southeastern part of the Baltic Sea, Fig. 1) is a shallow (the average depth is 3.8 m) eutrophic water basin connected to the Baltic Sea in the northern part. Because of frequent and unpredictable wind-induced sea water inflows, salinity varies from 0 to nearly 8 psu in the northern part of the lagoon (Þaromskis 1996). The littoral zone of the lagoon is characterised by a monotonous or a patchy vegetation cover pattern. Potamogeton perfoliatus and P. pectinatus are the dominant submerged vegetation species. Owing to high water turbidity and summertime cyanobacteria blooms (Plokðtienë 2002), their distribution is restricted to a depth of about 1 m. Zooplankton is dominated by the freshwater species Daphnia, Bosmina, Chydorus, Mesocyclops and Cyclops. Marine species (Acartia, Podon, Temora, Eurytemora) appeared only during inflows of brackish water (Gasiûnaitë 2000). The seasonal pattern of the freshwater Curonian Lagoon zooplankton community has been described by Gasiûnaitë and Razinkovas (2004). The mysid assemblage in the littoral zone of the lagoon consists of two introduced Ponto-Caspian species: Paramysis lacustris and Limnomysis benedeni. Figure 1. Study area. S1 S4: sampling sites. The sampling scheme indicates macrophyte beds (filled areas), zooplankton sampling stations (open circles) and traps (triangles) for each sampling transect. The actual macrophyte bed size and location are shown.

3 314 Lesutienë J., Gasiûnaitë Z. R., Grinienë E. P. lacustris prefers an open sandy-aleuritic bottom at a depth of 1 3 m, while L. benedeni is associated with submerged vegetation (Razinkovas 1996). The juvenile fish assemblage is dominated by smelt (Osmerus eperlanus L.) and pikeperch (Stizostedion lucioperca L.) in pelagic habitats, while roach (Rutilus rutilus L.) and perch (Perca fluviatilis L.) dominate in the littoral zone (Þiliukienë 1998; Þiliukas 2003). Sampling and sample treatment. We selected two sites in the comparatively narrow littoral zone with a characteristic steep slope and a well-defined submerged macrophyte distribution edge (S1 and S2) and two sites in the extended littoral zone with a patchy vegetation cover pattern (S3 and S4; Fig. 1). Zooplankton, juvenile fish and mysids were sampled on four occasions at the end of June (S1) and July (S4) 2001 and at the end of June 2002 (S2, S3). We collected six zooplankton samples at S1 all over the entire littoral-pelagic transect in the narrow littoral zone (depth ranged from 0.7 to 4 m, macrophytes concentrated in the narrow belt at a depth of m) and five samples at S4 in a randomly selected P. perfoliatus stand in the extended littoral zone (depth range at all sampling stations was m). These sampling transects have a distinctly different spatial scale ranging from hundreds of meters at S1 to only several meters at S4. To have more comparable data and avoid spatial differences due to depth and the dominance of other physical forces emerging on a larger scale (Folt & Burns 1999), we sampled two short transects with only two close stations in adjacent habitats. At S2 in the narrow littoral zone, a vegetated station was sampled at a depth of 0.8 m and an open station at a depth of 1.2 m, while at S3 in the extended littoral area, both stations were sampled at a depth of 0.7 m. Macrophyte coverage in all the vegetated habitats sampled in this study was no less than 80%. Distances between sampling stations and macrophyte locations in all the four transects are presented in the scheme (Fig. 1). Zooplankton was sampled at 12:00 a.m. (midday) and 12:00 p.m. (midnight) using a 10 l bathometer and a 100 µm mesh size plankton net. All samples were preserved in a 4% formaldehyde solution. Plankton crustaceans were identified, calculated and measured. Fish and mysid samples were collected simultaneously using two modified Breder traps with a funnel-like entrance (a square outer entry hole with an area of 0.42 m 2, a circular inner entry hole 0.15 m in diameter raised 0.2 m above the bottom) and a cone-shaped mesh container. Mysids could enter the trap only by swimming into the water column during nocturnal migrations. We chose Breder traps because towed nets proved inefficient in vegetation (Rozas & Minello 1997). We also refused to use the strongly recommendable enclosure samplers because they made gathering of small mysids from plants complicated and their application at night was difficult. However, we had to acknowledge that passive trapping also had disadvantages, low and variable catch efficiency being the main of them (Rozas & Minello 1997). Traps were set at the vegetation edge at a depth of 1 m at S1 and at a depth of m at S2, S3, S4. They were oriented to the opposite directions: one towards vegetation and another towards the adjacent open zone (Fig. 1). Sampling continued throughout the night (9:00 p.m. to 6:00 a.m.) and day (6:00 a.m. to 9:00 p.m.). Trap samples were collected every three hours. All daytime and nighttime samples were treated as replicates in further calculations. Juvenile fish and mysids were preserved in a 4% formaldehyde solution, identified and measured. Mysids were classified into two groups: a juvenile-size group (2 6 mm) and an adult-size group (>6 mm). Results were expressed as numbers of fish or mysids per trap or as a proportion of individuals caught in vegetation and open water. Juvenile fish diet analysis. No less than ten specimens per time period/habitat were dissected if available. Prey items counted in the entire fish intestine were identified to the genus (cladocerans and macroinvertebrates) or to the order (copepods, ostracods and amphipods). Each prey item was measured directly or reconstructed from typical remaining structures. The biomass of prey was calculated using allometric equations (Rumohr et al. 1987; Jorgensen et al. 1995). The diet data were averaged for day and night samples, leaving diurnal foraging cycles out of account. Empty intestines and those with more than 50% of unidentifiable food were excluded from the analysis (the total number of specimens used for the statistical diet analysis was 43 for pikeperch, 113 for perch, 70 for roach). No mysids were found in juvenile fish intestines. Statistical methods. We performed the analysis of the habitat effect on the mysid and juvenile fish distribution on the basis of the data pooled from three sampling sites. Prior to data pooling, we examined fish body length differences among sites/years and habitat types applying the Kruskall-Wallis test of medians on square root transformed length measurements. Proportions of each fish and mysid species in vegetated and un-vegetated habitats were calculated by summing-up simultaneous catches in two traps. Proportions in habitats were compared using a t-test for dependent samples or a nonparametric Wilcoxon matched pairs test if the data did not exhibit normality. In this study data normality was checked using the Kolmogorov-Smirnov test. The effect of the daytime on the abundance of certain fish species per catch was estimated by compar-

4 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 315 ing samples pooled from both habitats during the day and the night at each sampling site separately using a non-parametric Mann-Whitney U-test for analysis. Statistical tests were performed using the StatGraphics package. The percentage contribution of each dietary component to the total biomass of the fish intestine content was calculated and analysed using multivariate methods of the Primer 5.0 package. Components of zooplankton prey were analysed individually while zoobenthic species (such as amphipods, corixids, chironomids, ostracods, mysids) and leptodoras were pooled in one group (referred to as other food in further descriptions). The Analysis of Similarities (ANOSIM) was applied at each sampling site separately using the dietary proportion data of each species caught in vegetated or un-vegetated habitats at the same time as replicates (day or night). This test is expected to demonstrate whether significant differences in the diet composition are species-, habitator diurnal rhythm-dependent. The data were square root transformed and the Bray-Curtis similarity coefficients were calculated for this analysis. Significant R values of pair wise comparisons were used as the dissimilarity extent: the zero R value indicates no differences between groups while near to 1 R values mean that all samples within groups are more similar to one another than any samples from different groups. Additionally, the t-test or the Mann Whitney U-test was performed to check habitat-related differences in proportions of each planktonic prey group to the total zooplankton biomass of the food ingested. The p = 0.05 value was treated as an indicator of significance. Diurnal and habitat-related changes in the structure of zooplankton community in S1 and S2 transects were analysed using the ordination procedure by MDS, based on the Bray-Curtis similarity indices. RESULTS Structure of the juvenile fish assemblage. Only 0+ pikeperch (the mean standard length ±SE 21 ± 4.1 mm) was caught at the sampling site S1, which is closest to the pelagial zone. At all other sites the assemblage of juvenile fish consisted mainly of 0+ perch and 0+, 1+ roach (1+ roach was not found at S4). The Kruskall- Wallis median test showed no significant differences in the body length of 0+ perch (40.7 ± 0.6 mm, n = 256), and 1+ roach (65.9 ± 1.3 mm, n = 71) either between different sampling sites (p > 0.05) or vegetated vs. unvegetated habitats (p > 0.05). The body length of 0+ roach slightly varied with years and was greater in July 2001 (31 ± 0.91 mm) than in June 2002 (28 ± 0.56 mm, the Kruskall-Wallis median test, p < 0.05). In total, six individuals of non-planktophagous perch larger than 80 mm were caught and not included into the analysis. Other juvenile fish constituted less than 5% of fish catch. Fish habitat use and diurnal changes in catch size. In contrast to roach, which used both habitats with some insignificant preference for open zones (t-test, Table 1), the relative proportion of perch per trap was significantly higher in vegetated than open habitats. The proportion of pikeperch did not differ significantly between the two habitats. Table 1. Fish and mysid proportions in a vegetated versus an open water habitat, calculated as a species number per catch in a particular habitat divided by the sum of simultaneous catches in two traps in both habitats. Numbers are means ±SD calculated from the data pooled from four sampling sites (the t-test for dependent samples, the Wilcoxon matched pairs test (z) for S. lucioperca and L. benedeni); N the number of sample pairs in two adjacent habitats, p significance level; * only at S1, ** only at S4. Vegetated Habitat type Open N t, (z) p Juvenile fish S. lucioperca* 0.38 ± ± z = P. fluviatilis 0.62 ± ± t = R. rutilus 0.37 ± ± t = Adult mysids P. lacustris 0.66 ± ± t = L. benedeni 0.69 ± ± t = Juvenile mysids P. lacustris 0.76 ± ± t = L. benedeni** 0.78 ± ± z =

5 316 Lesutienë J., Gasiûnaitë Z. R., Grinienë E. The total number of the dominant juvenile fish in daytime catches differed significantly among sites (Kruskall-Wallis test, p < 0.05). Perch and roach were most abundant at S3 in the patchy littoral, but both of them were few at S4 in the analogous type of the littoral (numbers given in Table 2). Perch was more abundant in catches than roach at S2 and S3, but did not differ significantly at S4. The decrease in perch numbers per catch was significant at nighttime at S2 and S3 (the Mann Whitney U-test, p < 0.05; Table 2), but there was no time effect on roach catches. Pikeperch was more abundant during the day (54 ± 32 ind trap -1 ) than during the night (7 ± 4.4 ind trap -1 ). Fish diet. The diet composition of perch and roach differed significantly in the same habitat type at all the three sites, but food components contributing to dissimilarity varied distinctly. The diet of 1+ roach in the open habitat of S2 consisted mainly of chydorids and chironomid larvae with a substantial proportion of copepods, but did not include any Daphnia or Bosmina which were common in the intestine of perch (R veg = 0.23 for vegetation and R open = 0.27 for the open habitat, p < 0.05, the ANOSIM test, see Figures 2, 3 for proportion differences in the diet of perch and 1+ roach). The diet of perch differed significantly from that of 1+ roach (R veg = 0.21 and R open = 0.35, p < 0.05; ANOSIM) and from that of 0+ roach (R veg = 0.21, p = 0.07 and R open = 0.44, p < 0.05) at S3 with different contributions of daphniids and chydorids. Daphniids made up nearly 10% of the diet of 1+ roach and 46% and 23% of that of perch (numbers are given for vegetated and un-vegetated habitats respectively). Chydorids reached an average of 80% and 90% of the 0+ roach diet and 7% and 27% of the perch diet (Figs 2, 3). The diet content of 0+ roach consisted of Bosmina and Daphnia, chydorids and copepods at S4 (Fig. 3). In contrast to roach (R veg = 0.52, p < 0.01, R open = 0.19, p < 0.05, ANOSIM), small-bodied cladocerans were absent from the perch diet, which consisted predominantly of daphniids, copepods and benthic food. The missing columns in Figures 2 and 3 are due to the low number of fish per catch, insufficient to demonstrate the diet composition. The ANOSIM of zooplankton prey proportions in the daytime diet showed significant habitat-related differences in the diet of perch at S3 (R = 0.28, p < 0.01), in that of perch (R = 0.24, p < 0.05) and roach (R = 0.39, p < 0.05) at S4, and in the diet of pikeperch at S1 (R = 0.38, p < 0.01). The univariate comparison of separate zooplankton prey item proportions helped to detect a significant habitat effect on the plankton prey selection in each case. The proportion of daphniids was significantly higher in zooplankton ingested by perch in vegetation whereas the proportion of ingested copepods and chydorids was higher in the open habitat (the Mann Whitney U-test, p < 0.05) of S3 and S4 but did not differ significantly at S2 as was also shown by ANOSIM. Roach did not show any significant habitat-related foraging differences at S3 and S2, but ingested a significantly larger proportion of bosminiids in macrophytes of S4 (the Mann Whitney U-test, p < 0.05). The pikeperch diet consisted of a significantly higher proportion of daphniids in open areas, and a significantly higher proportion of bosminiids in vegetated areas (Mann Whitney U-test, p < 0.05). The ANOSIM confirmed day/nighttime differences in the pikeperch diet (R = 0.63, p < 0.01) caused by the shift from the domination of Daphnia at night to Bosmina during the day (Fig. 2). A significant difference in the Table 2. The Wilcoxon matched pairs test for the comparison of perch and roach (both 0+ and 1+) catches at three sampling sites (S2, S3, S4) in the daytime and at nighttime. Values are means ± SE ind/ trap; N the number of sample pairs; p significance level; n. s. not significant. S2 a site with the littoral macrophyte edge facing the open pelagic zone, sites S3 and S4 represent separate macrophyte beds in the patchy extended littoral zone. Perch N Roach N p Day S ± ± p < 0.05 S ± ± p < 0.05 S4 4.9 ± ± n. s. Night S2 3.0 ± ± n. s. S3 8.6 ± ± n. s. S4 2.5 ± ± n. s.

6 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 317 Figure 2. Variation in the diet composition of perch and pikeperch among stations and according to the time of the day in two habitat types: the first column in each pair shows the vegetated habitat-related diet, the second the diet associated with an un-vegetated habitat. Other prey items combine macrozoobenthos and Leptodora. Description of sampling sites S1 S4 as in Table 2. Figure 3. Variation in the roach diet composition among stations and according to the time of the day in two habitat types: the first column in each pair shows the vegetated habitat-related diet, the second the diet associated with an unvegetated habitat. Other prey items combine macrozoobenthos and Leptodora. Description of sampling sites S2 S4 as in Table 2. perch food ingested in macrophytes was induced by an increase in the average proportion of benthic food from 30% to 63% at S2 (R = 0.25, p < 0.01) and from 32% to 76% at S4 (R = 0.19, p < 0.03) at night compared to the daytime. Because of low roach catches at nighttime, diet proportions are not analysed statistically. Mysid assemblage. The abundance of mysids varied significantly among sites. Adults of P. lacustris dominated at three sampling sites, except S4, where L. be- nedeni and juveniles of both species were numerous as well. Mysids appeared to be most abundant in the water column between 12:00 p.m. and 3:00 a.m. The highest numbers of P. lacustris adult individuals were recorded in vegetation at all sites at that time (up to 900 ind trap -1 at S1, 500 ind trap -1 at S2, 70 ind trap -1 at S3 and 200 ind trap -1 at S4). The abundance of adult L. benedeni reached up to 200 ind trap -1 at S4 whereas it did not exceed 10 ind trap -1 at other sites.

7 318 Lesutienë J., Gasiûnaitë Z. R., Grinienë E. The proportions of both species, averaged for the three sites, were significantly higher in vegetation (Table 1). The juveniles of L. benedeni were found only at site S4 and reached 230 ± 26.6 on average in vegetation and 71 ± 23.7 ind trap -1 in the open zone. Distribution and composition of zooplankton. A clear diurnal pattern of both structural and quantitative characteristics of plankton crustaceans was observed at S1 (Fig. 4). Copepoda and Chydoridae dominated in the littoral zone, whereas Copepoda and Daphnia dominated in the pelagic zone during the daytime. All nighttime samples were pooled into one group, characterised by the highest relative abundance of Copepoda. The total density of littoral and pelagic zooplankton differed distinctly only during the day. Chydoridae dominated at S2 during the day and Copepoda during the night (Fig. 5). The total abundance was up to six times higher during the nighttime. A similar dominance pattern was found at S3. The total zooplankton abundance was 2.3 times higher during the day, and no quantitative differences were observed between the habitats. All nighttime samples and one daytime sample from the middle part of the macrophyte bed at S4 were pooled into one group due to the highest relative abundance of Copepoda (Fig. 6). The rest of daytime samples were characterised by a somewhat higher relative density of Daphnia. Figure 4. The MDS ordination of zooplankton samples at S1 based on relative zooplankton densities and the Bray- Curtis similarity. The diameter of the bubbles indicates the total crustacean density (from 7 to 76 ind/l). The bar chart represents the mean relative densities of the main zooplankton taxa for each group of samples. N night, D day, P pelagic zone, L littoral. Figure 5. Relative zooplankton densities at S2 and S3. N night, D day, V vegetated area, O open area.

8 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 319 Figure 6. The MDS ordination of zooplankton samples at S4 based on relative zooplankton densities and the Bray-Curtis similarity. The diameter of the bubbles indicates the total crustacean density (from 16 to 36 ind./l). The bar chart represents the mean relative densities of the main zooplankton taxa for each group of samples. N night, D day, E vegetation edge, M middle of the macrophyte bed, O open area. Traps were set at the vegetation edge marked with the number 2. DISCUSSION A significant differentiation between the vegetated and the adjacent open habitat by mysids during their nocturnal migrations was established. Similarly, juvenile perch showed a significant preference for vegetation. However, our estimates do not show any differences in roach and pikeperch distribution. Habitat-related feeding preferences of juvenile perch and roach as well as those of pikeperch basically differed in proportions of cladocerans in their diets. So in further discussions of the observed zooplankton horizontal heterogeneity both on a scale of a single macrophyte patch and the entire littoral-pelagic transect, we focused on the distribution of cladocerans. The tendency for 0+ perch to prefer vegetated habitats corresponds with the findings of previous investigations in artificial ponds and experimental enclosures. In previous investigations, this pattern was attributed to species-specific anti-predator and foraging capacities (Persson & Eklöv 1995; Jacobsen & Berg 1998). It was previously stated that perch is a more efficient feeder on zooplankton within vegetation when competing with roach (Diehl 1988; Persson & Eklöv 1995; Burks et al. 2001). Roach individuals possess better predator avoidance and escaping abilities, so they are able to forage in open areas or close to vegetation even in the presence of predators (Eklöv & Persson 1995; Eklöv & Van Kooten 2001). The ability of juvenile roach to shift frequently between habitats (Eklöv & Persson 1995) could explain insignificant roach proportion differences between open and vegetated habitats, observed in our study. Our results also suggest that differences in perch and roach foraging modes are habitat type-related. As it has been predicted, roach used the open space more efficiently when foraging on Daphnia in the patchy littoral zone (S4), while perch was at an advantage when foraging in vegetation (Figs 2, 3). Roach foraged predominantly on more abundant chydorids under the conditions of analogous littoral patchiness at S3 regardless of the habitat facilitation, while perch still managed to consume substantial amounts of Daphnia in vegetation, even though it was a minor contributor to the zooplankton community (Fig. 5). Habitat openness and decreased safety near the pelagic zone did not reduce the ability of roach to forage selectively on planktonic copepods. The percentage of copepods was higher in the diet of roach in open areas at S2, while benthic invertebrates prevailed in the diet of this fish in vegetation (Fig. 3). It is known that prey size selectivity can influence the partitioning of zooplankton prey resource, i.e. roach consume small-sized prey (represented by chydorids in this study), while perch is a superior forager on largesized daphniids (Thiel et al. 1996). The decline of daphniids leads to perch switching to a benthic food source during the first year of life (Mehner et al. 1995). Perch use the analogous strategy to compensate for the decreased availability of zooplankton prey in vegetation (Persson & Eklöv 1995; Wojtal et al. 2003). This pattern was evident at both patchy littoral sites (S2 and S4) at night. Similarly to the previous studies performed using passive fishing techniques, perch was more active and entered traps in higher numbers during the daytime, and roach

9 320 Lesutienë J., Gasiûnaitë Z. R., Grinienë E. numbers did not show such a significant decrease at night (Jacobsen & Berg 1998). Basically, this activity pattern is related to the fish feeding cycle: it has been shown previously that perch reduce food consumption in darkness (Diehl 1988; Granquist & Mattila 2004), while roach is known to be a less light limited forager (Haertel & Eckmann 2002). This could explain diurnal differences between our catches of perch and roach (Table 2). However, in this respect it is necessary to note the possible effect of sampling gear selectivity, which may lead to low roach catches as compared to those of perch (Table 2). The problem of low roach catches using the Breder trap was stated in previous experiments as well (Jacobsen & Berg 1998). However, the recent study of the Curonian Lagoon littoral juvenile fish community using the beach seine (Þiliukas 2003) reported quite similar proportions of perch and roach: 80% and 20% in vegetated habitats (compared to on an average 77% and 23% in this study) and 46% and 54% respectively in open littoral areas (compared to 50% and 50% in this study). Pikeperch, documented as a typical species of the juvenile fish assemblage in the pelagic zone of the Curonian Lagoon (Þiliukienë 1998), differentiated between open pelagic water and vegetated habitats significantly (at S1). In the pelagic zone, pikeperch fed predominantly on the most widely available Daphnia, while in littoral vegetation, pikeperch shifted to smaller Bosmina (Figs 2, 4). It was observed that pikeperch, which preferred deeper habitats with lower predator pressure to upper water strata with abundant larger cladocerans available for food (Frankievicz et al. 1998), shifted from particulate to filtering feeding on small-sized prey. The shift in pikeperch feeding mode from an open to a vegetated habitat, reported in our study, may be also related to the reduced efficiency of particulate feeding on larger cladocerans in vegetation. The tendency of mysids to aggregate in vegetated habitats and disperse in the water column during nocturnal migrations was typical of both mysid species and size groups (Table 1). Owing to their ability to forage on larger prey, adult mysids are supposed to be more important feeders on zooplankton than juveniles. Food particle size selected by juveniles can reach up to 350 µm, while adults ingest prey ranging from 100 to 1,700 µm (Jankauskienë 2001). Therefore, during their nocturnal migrations, adult mysids are capable of foraging on many zooplankton species excluding large Daphnia and Leptodora. The increased survival of zooplankton in littoral macrophyte refuges during the daytime is one of the main forces determining the horizontal distribution of zooplankton (Lauridsen & Buenk 1996; Jeppesen 1998; Folt & Burns 1999). During the day the community structure and density of zooplankton in vegetated and open habitats in the patchy littoral of S3 and at the littoral vegetation edge of S2 were similar although fish juveniles were expected to avoid open pelagic waters. This fact supports the idea of a complete vegetation refuge loss under the combined predatory effect of perch and roach. As it has been stated in previous studies, roach were a serious threat to Daphnia in the open zone, but they had a weak impact on prey resources in vegetation due to ineffective foraging in this habitat (Burks et al. 2001; Eklöv & Van Kooten 2001). In contrast, it has also been stated that Daphnia gain incomplete refuge from fish predation even in dense vegetation and tend to aggregate in offshore open water zones (Kairesalo et al. 2000; Nurminen & Horppila 2002), particularly in the presence of juvenile perch (Burks et al. 2001) or invertebrate predators (Smiley & Tessier 1998). The ability of macrophytes to serve as a refuge for zooplankton is related to fish densities: densities higher than 2 ind m -2 can completely eliminate the refuge effect (Jeppesen 1998; Bertolo et al. 1999). The refuge effect on zooplankton distribution is hardly expected in the littoral zone of the Curonian Lagoon because fish aggregations with densities of YOY higher than 10 ind m -2 can appear in June and July (Repeèka et al. 1996). Nevertheless, an increase in the relative abundance of daphniids was indicated in vegetation and at vegetation edges at S4 while exploring the entire P. perfoliatus bed during the day (Fig. 6). We noticed that the lowest total catch size of juvenile fish was recorded at S4 (Table 2). Besides, the macrophyte edge was previously observed as the most attractive zone for cladocerans balancing the need for macrophyte refuge with the avoidance of macrophyte chemical cues (Lauridsen & Buenk 1996). Clear habitat segregation by zooplankton was also observed in the littoral-pelagic transect at S1. Reduced total abundances in all littoral habitats and the aggregation of Daphnia in the open pelagial zone during the day (Fig. 4) could be interpreted as a result of juvenile fish feeding in the littoral zone. However, we have to be cautious about this interpretation. Actually, pikeperch sampled at the vegetation edge at S1 represent a pelagic but not a littoral juvenile fish assemblage. Therefore, the extrapolation of its feeding influence on the whole littoral is somewhat unjustified. Besides, hydrodynamic processes, which are not evaluated in this study, could have an additional effect on zooplankton heterogeneity in the transect S1 as it has the largest spatial scale (Fig. 1). It is supposed that individual behavioural patterns or patchiness induced by predators by removing individuals can be more important for zooplankton heterogeneity than

10 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 321 physical forces on a spatial scale from 1 mm to 10 m while on larger scales they tend to have a combined effect (Folt & Burns 1999). We could conclude that differences in juvenile fish foraging in vegetated and adjacent open habitats, capable of creating spatial heterogeneity in the daytime, appear to be less important for zooplankton dispersal at night due to reduced fish activity. Almost homogeneous zooplankton distribution at night at most research sites (S1, S3 and S4, Figs 4, 5 and 6) also suggests the absence of the structuring macrophyte effect under the influence of mysids, although mysids showed a clear tendency to aggregate in vegetation during their nocturnal migrations. In this study we did not consider hydrodynamics and water chemical parameters as important factors in creating environmental vegetationrelated heterogeneity. Nevertheless, summarising the results on the daytime zooplankton heterogeneity, we could emphasize several features of the cladoceran distribution: the tendency to be more abundant in the pelagial zone and to avoid littoral vegetation (S1), the loss of vegetation refuge in the patchy littoral as a result of combined predation by juvenile perch and roach (S3) and the ability to gain spatial refuge in macrophytes or at the edge of vegetation (S4) when juvenile fish abundance is low. ACKNOWLEDGEMENTS We thank Darius Daunys for suggestions on statistical analysis and Lisa Rima Bacanskas for careful reading and language revision. This work was partly funded by EU FP 5 project COLAR (EVK3-CT ). REFERENCES Bertolo, A., Lacroix, G., Lescher-Moutoue, F. and Sala, S Effects of physical refuges on fish-plankton interactions. Freshwater Biology 41: Burks, R. L., Jeppesen, E. and Lodge, D. M Littoral zone structures as Daphnia refugia against fish predators. Limnology and Oceanography 46: Carpenter, S. R. and Lodge, D. M Effects of submerged macrophytes on ecosystem processes. Aquatic Botany 26: Diehl, S Foraging of three freshwater fishes: effects of structural complexity and light. Oikos 53: Donk, E. van and Bund, W. J. van de Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: Eklöv, P. and Persson, L Species-specific antipredator capacities and prey refuges: interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). Behavioral Ecology and Sociobiology 37: Eklöv, P. and Van Kooten, T Facilitation among piscivorous predators: effects of prey habitat use. Ecology 82 (9): Folt, C. L. and Burns, C. W Biological drivers of zooplankton patchiness. Tree 14: Frankiewicz, P., Zalewski, M., Schiemer, F. and Dabrowski, K Vertical distribution of planktivorous 0+ pikeperch, Stizostedion lucioperca (L.), in relation to particulate or filter feeding. Fisheries Management and Ecology 4: Gasiûnaitë, Z. R Coupling of the limnetic and brackish water plankton crustaceans in the Curonian Lagoon (Baltic Sea). International Revue of Hydrobiology 5 6: Gasiûnaitë, Z. R. and Razinkovas, A Temporal and spatial patterns of crustacean zooplankton dynamics in transitional lagoon ecosystem. Hydrobiology 514: Granquist, M. and Mattila, J The effects of turbidity and light intensity on the consumption of mysids by juvenile perch (Perca fluviatilis L.). Hydrobiology 514: Haertel, S. S. and Eckmann, R Diel diet shift of roach and its implications for the estimation of daily rations. Journal of Fish Biology 60: Jacobsen, L. and Berg, S Diel variation in habitat use by planktivores in field enclosure experiments: the effect of submerged macrophytes and predation. Journal of Fish Biology 53: Jankauskienë, R Trophic relations of the Ponto- Caspian higher crustaceans and fish larvae in the littoral zone of the Curonian Lagoon. Ph. D. thesis. [Jankauskienë, R Ponto-Kaspijos aukðtesniøjø vëþiagyviø bei þuvø lervø trofiniai ryðiai Kurðiø mariø litoralëje. Daktaro disertacija.] Jeppesen, E The ecology of shallow lakes trophic interactions in the pelagial. NERI Report 247: 22, 25. Ministry of Environment and Energy, National Environmental Research Institute, Silkeborg, Denmark. Jeppesen, E., S ndergaard, M. and Christoffersen, K. (eds) The Structuring Role of Submerged Macrophytes in Lakes. Ecological Studies 131: 423. New York: Springer. Jorgensen, S. E., Nielsen, S. N. and Jorgensen, L. A Handbook of ecological parameters and ecotoxicology. Amsterdam-London-New York-Tokyo: Elsevier. Kairesalo, T., Kornijow, R. and Luokkanen, E Trophic cascade structuring a plankton community in a

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12 Habitat-induced heterogeneity in the Curonian Lagoon littoral assemblages 323 pø ir jø planktoniná maistà daþnai sudaro smulkûs chidoridai, taèiau pastebëta ir didesnë dafnijø bei irklakojø vëþiagyviø proporcija neapaugusiuose biotopuose nei augmenijoje. Ponto-Kaspijos mizidës (Paramysis lacustris) ir (Limnomysis benedeni) naktiniø migracijø metu gausiau telkiasi augmenijoje. Taèiau nepastebëjome akivaizdaus jø poveikio zooplanktono pasiskirstymui tarp dviejø biotopo tipø nakties metu. Didesnis zooplanktono horizontalaus pasiskirstymo heterogeniðkumas pasireiðkia dienà. Iðskyrëme keletà ypatybiø bûdingø ðakotaûsiø vëþiagyviø horizontaliam pasiskirstymui augmenijos bei þuvø jaunikliø mitybos elgsenos atþvilgiu. Norint iðsamiau apraðyti Kurðiø mariø litoralës zooplanktono pasiskirstymà reikëtø ávertinti ir hidrodinaminius veiksnius. Received: 6 June 2005 Accepted: 16 November 2005