Distribution of the Non-Indigenous Cercopagis Pengoi in the Coastal Waters of the Eastern Gulf of Finland

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ICES Journal of Marine Science, 56 Supplement: 49–57. 1999 doi:10.1006/jmsc.1999.0613, available online at http://www.idealibrary.com on

Distribution of the non-indigenous Cercopagis pengoi in the coastal waters of the eastern Gulf of Finland

A. Uitto, E. Gorokhova, and P. Va¨lipakka

Uitto, A., Gorokhova, E., and Va¨lipakka, P. 1999. Distribution of the non-indigenous Cercopagis pengoi in the coastal waters of the eastern Gulf of Finland. – ICES Journal of Marine Science, 56 Supplement: 49–57.

We studied the distribution and population structure of the immigrant predaceous cladoceran species Cercopagis pengoi and its role in the zooplankton community during a 1-week cruise at the beginning of September 1997. Samples were collected at 20 stations within a coastal area of 500 km2 in the Gulf of Finland. Temperature above the thermocline was about 16–18C. Phytoplankton was dominated by filamentous blue-green algae, metazooplankton by rotifers, cladocerans, cyclopoids, and calanoids. Ciliates (maximum density 2105 L1) were dominated by oligotrich ciliates and Mesodinium rubrum. The maximum density of different metazoan taxa varied from a few (Cercopagis) to a thousand (rotifers) per litre. Most of the Cercopagis population consisted of maturing parthenogenic females with a low percentage of males and gametogenic females. On the basis of population structure, we suggest that the population was still in the growth phase, parthenogenesis being the dominant reproduction strategy. Variation in zooplankton community structure and density was associated with differences in salinity, the stations nearest to the coast favouring cladocerans and cyclopoids. Rotifers and ciliates were most abundant at the eastern stations. Since density of Cercopagis was also highest at the eastern stations, this predator may have been an important factor in the structure of the zooplankton community. The potential effects of Cercopagis on the pelagic community structure and dynamics in the Gulf of Finland are discussed.

1999 International Council for the Exploration of the Sea

Key words: Baltic Sea, Cercopagis pengoi, non-indigenous species.

A. Uitto: Department of Ecology and Systematics, Division of Hydrobiology, P.O. Box 17, FIN-00014 University of Helsinki, Finland; E. Gorokhova: Department of Systems Ecology, Stockholm University, 109 61 Stockholm, Sweden; P. Va¨lipakka: Southeast Finland Regional Environment Centre, P.O. Box 1023, FIN-45101 Kouvola, Finland

Introduction decline in local anchovy fisheries through heavy predation on zooplankton and food competition with native Anthropogenic activities have been the main cause of fish (Vinogradov et al., 1989; Shushkina and Museva, non-indigenous species being introduced to new areas in 1990). the last century (Carlton, 1989), and in aquatic ecosys- While the Baltic Sea has been the destination area tems shipping has enabled the invasion of species that of tens of non-indigenous fish and benthic species survive in ballast water and find areas similar to their (Leppa¨koski, 1984, 1991), only two newcomer zoo- native habitats (Carlton and Hodder, 1995). Introduced plankton species are known to be abundant: the cala- or accidentally spread zooplanktivorous fish, mysid noid copepod Acartia tonsa Dana (Leppa¨koski, 1984) shrimps, and predaceous cladocerans are known to and the cladoceran Cercopagis pengoi (Ostroumov) affect the structure and functioning of the receptive (Ojaveer and Lumberg, 1995). The appearance of the pelagic ecosystems in lakes (Brooks and Dodson, 1965; latter represents the most recent recorded invasion. Cooper and Coldman, 1980; Lehman and Caceres, Cercopagis is endemic to the Ponto–Aralo-Caspian 1993). Human-mediated introductions in marine areas basin, occurring in the Caspian, Black, Aral, and Azov have been less studied (Carlton, 1996). The introduction seas, their estuaries, coastal lakes, and in cascading of Mnemiopsis leidyi (Ctenophora), a planktivorous reservoirs on the Don and Dnieper rivers (Mordukhai- North Atlantic comb jelly, to the Black and Azov Seas Boltovskoi and Rivier, 1987). In the Baltic Sea, Cerco- has caused a decrease in zooplankton biomass and a pagis was first found in the Pa¨rnu Bay and Gulf of Riga

1054–3139/99/060049+09 $30.00/0 1999 International Council for the Exploration of the Sea 50 A. Uitto et al. in 1992 (Ojaveer and Lumberg, 1995). In August 1995, course of one week in September 1997 (Fig. 1). The the species was identified in samples taken in the coastal stations extended from the archipelago into open sea area off Kotka, Gulf of Finland. In September 1995 and areas with increasing salinity and decreasing tempera- 1996, it was found in the Neva estuary and in the open ture offshore. The vertical hydrography was studied sea area of the eastern Gulf of Finland (Avinski, 1997). using a SIS CTD-plus 100 with a measurement interval In 1997, the species appeared also in the Baltic Proper of 0.5 m. (Gorokhova, 1998) and in the Asko¨ area (N. Aladin, Water samples for Chl a and ciliate analyses com- pers. comm.). bined were collected with a Ruttner water sampler from Information on Cercopagis is largely taxonomic or depths of 1, 2.5, 5, 7.5, and 10 m. Chl a samples were zoogeographic (see Mordukhai-Boltovskoi and Rivier, filtered on GF/F filters onboard and immediately deep- 1987). Anatomo-morphological description of embryo- frozen for later measurement in the laboratory. Ciliate and gametogenesis as well as fecundity of cercopagids samples of 200 ml were preserved in acidic Lugol solu- has been reported by Rivier (1969). As is the case in tion. Phytoplankton samples were collected using a many cladoceran species, parthenogenic breeding is an 20-m mesh net from 10 m depth to the surface and also important and sometimes the only reproduction strat- preserved in acidic Lugol solution. Mesozooplankton egy. Parthenogenic females usually comprise the bulk of samples were collected using a 100-m plankton net the population with few males and gametogenic females. (opening diameter 28 cm). To study Cercopagis distribu- The latter carry one or two resting eggs (Modukhai- tion, samples were taken only during daylight hours Boltovskoi and Rivier, 1987). Demographic and life- from three water layers: 0 to 10 m (all stations), 0 to history parameters from both native and receptive areas 25 m (station numbers 4, 14–16, and 19), and from the are sketchy and relate mostly to reproduction activity whole water column (station numbers 1–4, 6–12, 14, and and size compositions (Mordukhai-Boltovskoi, 1967, 18; Fig. 1). The net was rinsed five times in surface 1968; Glamazda, 1971; Mordukhai-Boltovskoi and water. Samples were preserved in 1-litre bottles with Galinsky, 1974). There is very little information on sea- heksamethyl-tetramin buffered 5% formaldehyde. sonal abundance, horizontal distribution, swimming be- Phytoplankton, ciliates, and rotifers were enumerated haviour, and vertical migration patterns in the Caspian using inverted microscopy. Phytoplankton abundance Sea (Rivier, 1968; Rivier and Mordukhai-Boltovskoi, was determined using the following scale: 1 – few cells, 1966; Glamazda, 1971). Although Cercopagis is known 2 – sparse, 3 – scattered, 4 – abundant, and 5 – to be a predator (Mordukhai-Boltovskoi and Rivier, dominant. Ciliates were enumerated quantitatively. 1987) feeding on copepods (Rivier, 1968) and other small They were identified mostly at the genus level and zooplankters, neither diet composition nor consumption biovolumes were measured by size group. Copepods and rates have been reported. Physiological characteristics cladocerans were enumerated from mesozooplankton appear not to have been studied. The scarcity of infor- subsamples of 50 ml under a dissection microscope. mation for an invertebrate predator limits our under- Cercopagis was counted in the entire samples and indi- standing of its ecological importance in a food web. viduals were stored in ethanol in plastic tubes for later Ever since its appearance in the Baltic Sea, Cercopagis examination of population structure and dry weight has become the subject of studies on distribution (DW) measurement. The biovolume of copepods and (Avinski, 1997; Gorokhova, 1998), seasonal abundance cladocerans was estimated using published values from (Krylov et al., in press), reproduction (Krylov and the northern Baltic Sea (Hernroth, 1985; Viitasalo, Panov, 1998), morphology (Simm and Ojaveer, 1999), 1992), Biovolumes were subsequently converted to car- and feeding (Gorokhova, 1998). The species has been bon, assuming a carbon content of 5.2% for copepods, found to be an important food item for pelagic and cladocerans, and rotifers (Mullin, 1969) and 11% for littoral fish species such as herring, three-spined and ciliates (Edler, 1979). The carbon content of Cercopagis nine-spined stickleback in the Gulf of Riga (Ojaveer was calculated assuming the DW to carbon percentage and Lumberg, 1995). We provide new information on of 44% found for other cladocerans (Hessen, 1990). its population structure and reproduction, as well as on To study horizontal differences in the planktonic its horizontal distribution in relation to abiotic and community, the sampling stations were classified as biotic parameters in the Gulf of Finland. We also discuss archipelago stations (nos. 2–3, 8–11, and 20) or sea area its potential role in the pelagic food web on the basis of stations (nos. 1, 4–7, 12–19) in accordance with the energy calculations. hydrography and the classifications of Haÿreń (1931). Taking into account information on prevailing water currents, nutrient concentrations, and eutrophication Materials and methods (Pitka¨nen et al., 1993), stations 1–8 and 16–20 were also grouped to represent the less eutrophied western Samples were collected at 20 stations within a coastal part, and stations 9–14 the more eutrophied eastern area of 500 km2 offshore of the town of Kotka in the part. Cercopagis pengoi in the waters of the eastern Gulf of Finland 51

27° Hamina

60°30' Kotka 20 * * (12) 8 (28) * Loviisa 9 11 (36) (26) * * 3 * 10 (23) * 7 (36) 2 (34) 12 (19) (51) 1 (42) 6 4 5 (18) (12) Transect 1 (42) 13 Transect 2 (62) 15 (53) 14 Study area 16 (64) (41) 19 (36)

17 (48) 18 0 1 2 3 4 5 10 km (16) Suursaari

Baltic Sea

Figure 1. Study area and sampling stations in the eastern Gulf of Finland during a 1-week cruise at the beginning of September 1997. Station numbers (depth in parentheses) indicate the sampling order (solid lines: two transects used for hydrography description of the area; hatched lines: split between western and eastern parts).

For population and DW analysis of Cercopagis, gen- Results der and reproductive stage of the animals were determined microscopically. The four classes typical for Owing to calm weather conditions, a strong thermal Cercopagidae (Mordukhai-Boltovskoi and Rivier, 1987) stratification prevailed in the entire study area. The were distinguished: neonates (N) represent newly thermocline was found in the 15–20 m depth range. The released individuals whose sex could not be determined; upper layer was fairly uniform, with temperatures males (M) belong typically to second instars or adults; between 16 and 18C, while the near-bottom water parthenogenic females (PF) of any age with embryos at temperature at depths >40 m was 3C(Fig. 2a, c). different stages of embryogenesis; and gametogenic Salinity varied from 2 to 7 psu, being lowest at the females (GF) of any age with resting eggs. Age-specific shallow nearshore stations and highest in the outer and morphological stages (or barb stages; BS) were distin- deepest stations (Fig. 2b, d). guished by the number of lateral spines (paired barbs) at The density of Cercopagis varied generally between 70 the base of the chitinous caudal appendage. The number and 350 m3, with an outstanding value of about 1800 of spines is age-related with one pair in neonates (first ind m3 at station 15 (biomass 45 mg DW m3; Fig. 3). instar or BS I) and a new pair added at each moult as the The additional vertical samplings conducted at some animals grow through the second instar (BS II) to a total stations over the entire water column and from 25 m of three pairs in adults (BS III). depth to the surface revealed that the vertical distribu- For determination of DW, three to five individuals of tion is patchy (Fig. 4). Clearly, the larger part of the the same barb stage and maturity for BS II and BS III, total population must have been present below a depth or 10 individuals for neonates, were placed in of 10 m at stations 4, 7, 9, 12, 18, and 19, while at pre-weighed tin capsules, dried over 24 h at 60C stations 1–3, 6, 8, 10, 11, and 14–16 the numbers caught and weighed on a Sartorius M3P microbalance in the surface layer of 10 m were roughly similar or (0.001 mg). Since DW of zooplankters decreases with higher than those caught over larger depths (Fig. 4). time in both formalin and ethanol, we assumed the Maturing parthenogenic females and neonates con- shrinkage effect for cercopagids to be the same as for tributed 60% and 28% of the population, respectively, ethanol-preserved daphniids (maximal value 53%; while males represented about 10% and gametogenic Campbell and Chowfraser, 1995). Thus, a coefficient females less than 3% (Table 1). The highest demographic 2.13 was applied to calculate DW of live animals. variability among sampling sites was observed in the 52 A. Uitto et al.

ff Transect 1, station no. ences in demographic parameters, only the di erence 19 42320in proportion of BS III between eastern (13 6.3, 16 16 medianSD) and western (2611.2) stations was 10 16 16 20 12 12 significant (Mann-Whitney t-test; p<0.05, U=19.50). 8 8 30 A Mean DW varied between sexes and developmental 4 4 40 stages and also within each stage (Fig. 6). Significant

Depth (m) ff °C di erences (Mann-Whitney t-test, p<0.05) were observed between neonates (0.00840.0019; median 19 42320 3 values SD) and older instars (0.048 0.019), between 4 10 adult males (0.0250.011) and those of second 5 20 5 instars (0.015 0.0021), and between adult males 30 6 6 B (0.025 0.011) and females (0.058 0.008). No signifi- 40 cant differences were found between gametogenic and Depth (m) psu parthenogenic females of the same developmental stage for either BS II (0.0550.009 and 0.0460.015, Transect 2, station no. respectively) or BS III (0.0610.005 and 0.0560.006, 18 17 16 14 15 10 9 respectively). Because of high variability in DW within ff 10 BS II, di erences between two-barb and three-barb 13 8 13 20 8 animals were not significant. 30 3 C 3 Filamentous blue-green algae dominated the phyto- 40 plankton at all stations. The blooming species was

Depth (m) 50 ° Aphanizomenon flos-aquae (L.), but the genus Anabaena, 60 C Oscillatoria, and Nodularia were also rich in numbers. 18 17 16 14 15 10 9 The concentration of Chl a varied from 3.8 to 7.2 g 4 10 l1. The highest concentration was found in the eastern 20 5 5 5 part at stations 10 and 11, the lowest near Kotka and the 30 6 D 6 6 estuary of the river Kymijoki (Fig. 7a). 40 7 Depth (m) 50 With the exception of two western archipelago sta- 60 psu tions, density and biomass of copepods exceeded those of cladocerans (Fig. 7b). Copepods were dominated by Figure 2. Temperature (A, C; C) and salinity (B, D; psu) profiles along the transects (cf. Fig. 1) in the western (A–B) and Mesocyclops leuckarti Claus, Acartia bifilosa Giesbrecht, in the eastern area (C–D). and Eurytemora affinis (Poppe). Bosmina longispina mar- itima (P. E. Mu¨ller) was the most common cladoceran species. Daphnids (mostly Daphnia cucullata Sars) and 2000 Evadne normanni Loveń occurred frequently at all Western Eastern 40 1500 stations. Cercopagis dominated metazoan biomass at 30 station 15 (Fig. 7b). Keratella spp., especially K. coch- N 1000 B learis (Gosse), was the most numerous rotifer at all 20 stations. Other species of the genus were K. quadrata 500 10 (Mu¨ller) and K. cruciformis var. eichwaldi (Levander). Synchaeta monopus dominated rotatorian biomass 0 0 1 2 3 4 19208 7 6 5 1617181112131415109 (Fig. 7c). AA AA A AA The dominant ciliates were classified according to sub- Station no. orders Haptorina (Didinium, Monodinium, and Meso- dinium), Oligotrichina (Strobilidium and Strombidium) Figure 3. Density (N individuals m3; columns) and biomass and others (Fig. 7d). The genus of Strobilidium, Strom- (BmgCm 3; diamonds) of Cercopagis pengoi by station (A: archipelago station; hatched line splits western and eastern bidium, and Mesodinium dominated ciliate abundance stations). and biomass. The Mann-Whitney one-tailed U-test showed that densities of cladocerans (p=0.003), cyclopoids (p=0.03), abundance of gametogenic females and males, while and total Copepoda (p=0.02) were higher in nearshore numbers of parthenogenic females were more consistent stations than in open sea stations. Furthermore, the (Fig. 5a). Higher prevalences of second and first instars densities of Cercopagis (p=0.03), Synchaeta spp. were observed than for adults (Fig. 5b). The CV (p=0.05), total Rotatoria (p=0.05), and Haptorina cili- increased with decreasing proportions of the barb stages ates (p=0.02) were higher in the eastern stations than in in the population (Table 1). In analysing regional differ- the western ones. Cercopagis pengoi in the waters of the eastern Gulf of Finland 53

Eastern Western

1400 1200 1000 800 600 400 200 Individuals per sample 0 9 15 10 14 A A Whole water 12 13 column 18 11 16 17 A 0–25 m 6 5 8 7 20 19 A 0–10 m 4 A 2 3 1 A Station number A Figure 4. Number of Cercopagis pengoi individuals in vertical samples taken from diﬀerent depths by station (A: archipelago stations).

Table 1. Mean percentage composition, standard deviation (s.d.), and coeﬃcient of variation (CV in %) of the population of Cercopagis pengoi by sex and age classes for the western and eastern areas separately and combined, September 1997 (N: neonates; PF: parthenogenic females, GF: gametogenic females; M: males; BS I–III: barb stages).

Sex Age N PF GF M BSI BSII BSIII

Western stations Mean 27.3 59.6 2.8 10.3 31.3 44.8 24.2 s.d. 12.2 13.6 3.1 8.1 14.1 10.3 11.2 CV 44.6 22.9 111.4 78.8 44.9 23.0 44.3 Eastern stations Mean 29.0 60.6 2.6 7.9 44.1 41.3 14.6 s.d. 16.5 13.8 2.2 4.4 14.5 12.9 6.3 CV 56.8 22.8 86.5 56.2 32.9 31.3 43.6 Overall Mean 27.9 60.0 2.7 9.4 37.8 42.0 20.4 s.d. 13.4 13.3 2.8 7.0 16.0 10.9 10.6 CV 48.1 22.2 102.0 74.3 42.2 26.0 51.9

3 Discussion wet weight m has been reported (Modukhai- Boltovskoi and Rivier, 1987), which, if converted to Cercopagis pengoi appears to have been successful in carbon with a carbon to wet weight percentage of 5.2% establishing a permanent population in the Baltic Sea. (26 mg C m3), is comparable to the maximum value The average density of 300 ind m3 (biomass estimated here based on DW (20 mg C m3). 4mgGm3) in the upper water layer were higher than Neonates and parthenogenic females comprised the the maximum values of 90 m3 reported by Krylov majority of the population. The low percentage of males et al. (in press) for September 1995 and are comparable and gametogenic females suggests that the population to the Caspian Sea (up to 350 m3; Rivier and in early September was still in the growth phase, Mordukhai-Boltovskoi, 1966). High densities as parthenogenesis being the basic reproduction strategy. observed at station 15 have also been recorded in Low sexual reproduction activity has also been men- Kakhovka Reservoir (1400 m3; Tseeb, 1962). In open tioned for native areas (Rivier, 1969). In contrast, Panov areas of the Azov Sea, a maximum biomass of 500 mg et al. (1996) observed that about 60% of the Cercopagis 54 A. Uitto et al.

A Western Eastern higher predation pressure on juveniles in the western 100 part, or favourable feeding conditions in the eastern part resulting in higher reproduction success. 80 Because ontogenetic development from birth to pri- maparity has not been described for Cercopagis species 60 and data on sexual maturation in relation to growth are

% also lacking, our observations may be compared with 40 those of another cercopagid, Bythotrephes cederstroemii Schoëdler. This species has been studied extensively 20 since its invasion of the Great Lakes (Yurista, 1992). Females with two and even one pair of barbs bearing 0 1 2 3 4 19208 7 6 5 1617181112131415109 embryos and gametogenic females with two pairs have N PF GF M often been observed in both species. Bythotrepes from reservoirs in The Netherlands were also fertile in the first B developmental stage (Ketelaars et al., 1995). Occasional 100 moults without adding barbs have been suggested as a possible explanation for this phenomenon, in which case 80 the number of barbs would not necessarily correspond to actual instars (Yurista, 1992). The extent to which 60 feeding conditions affect moulting frequency and barb

% formation remains unknown. Although we observed 40 both mature females and males with two pair of barbs in all samples, and age stages appear to be virtually the 20 same for both species, it is unclear whether reproduction occurs at this stage or is postponed until the final stage is 0 1 2 3 4 19208 7 6 5 1617181112131415109 reached. BS I BS II BS III The variation in DW within the second instar, which is composed of males and females, was high, indicating Figure 5. Population structure of Cercopagis pengoi: (A) by sex that individuals of very different size are able to mature. class (N: neonates; PF: parthenogenic females; GF: gametogenic females; M: males); (B) by age class (BS: barb stage). Variability in maturation may be a sign of rapid adap- tation to favourable conditions, a common feature among freshwater cladoceran species such as daphniids, and which allows them to respond to environmen- GF tal variation, both phenotypically and genotypically PF (Korpelainen, 1985; Lampert and Sommer, 1997). These BS III features, combined with parthenogenesis allowing rapid M population growth, could mean that this non-indigenous species readily adapts to recipient ecosystems. GF BS II According to a preliminary study (Gorokhova, 1998), PF the diet of Cercopagis in the northern Baltic Proper in 1997 consisted of 60% copepods (nauplii and copep- M odites of the genus Acartia, Eurytemora, and Temora), N BS I 20% rotifers (Synchaeta baltica), and 20% podonids (Evadne nordmanni). Marshall (1973) estimated that at 0 0.02 0.04 0.06 0.08 10C the carbon requirement of copepods for daily Dry weight (mg) maintenance, without the extra energy needed for Figure 6. Variation in stage-specific dry weight (mg) of instance for reproduction and vertical migration, was Cercopagis (cf. Fig. 5). 5–15% of body carbon. Specific respiration increases with temperature (Omori and Ikeda, 1984) and at 20C daily maintenance may be even 25% of body carbon population on the north-eastern coast of the Gulf of (Marshall, 1973). Assuming similar percentages for Finland in late summer 1996 consisted of gametogenic Cercopagis at a surface temperature of 18C, it would females. A larger proportion of adult animals was found have consumed daily on average one-tenth of metazoo- in the western part compared to the eastern part. Since plankton biomass for maintenance alone, and the maxi- abiotic conditions were fairly uniform over the area, two mum biomass observed at station 15 about one-third. possible biotic mechanisms might explain this difference: This indicates that a dense Cercopagis population may Cercopagis pengoi in the waters of the eastern Gulf of Finland 55

A Western Eastern have patchy eﬀects on the metazooplankton in the Gulf 10 of Finland within days. When the additional carbon )

1 8 – need for somatic growth and reproduction is included, g l

µ 6 the actual consumption was probably even greater. 4 The average biomass of calanoid copepods and cladocerans was within the range reported by Pitka¨nen Chl. a ( Chl. 2 ND et al. (1993) for the area, but that of rotifers and ciliates 0 1 2 3 4 19 20 8 7 6 5 16 17 18 11 12 13 14 15 10 9 was several times larger. Compared with the long-term B-1 average in the Gulf of Finland in early September on the 100 basis of hydrographical data (Haapala and Alenius, Cercopagis pengoi

3 Cladocera 1994), the temperature of the upper water layer in 1997

– 80 Copepoda nauplii m was several degrees higher. Also, the upper water col- 3 60 Cyclopoida umn was fairly homogeneous due to prevailing calm 10 Calanoida

× 40 whether conditions. Since many rotifer, cladoceran, and

Ind 20 cyclopoid species in the Baltic Sea prefer stable condi- 0 tions, high temperatures, and low salinity (Viitasalo B-2 50 et al., 1995), the abiotic conditions were probably responsible for the high abundance of these groups. 40 3

– Cercopagids are considered typical warm-water species. 30 In the Caspian Sea, Cercopagis appears in the water 20 column when temperature rises above 17C and disap- mg C m 10 pears when it drops below 13–16C(Rivier and 0 Mordukhai-Boltovskoi, 1966). In the Baltic Sea, the 1 2 3 4 19 20 8 7 6 5 16 17 18 11 12 13 14 15 10 9 density increased during calm water conditions at a C-1 temperature of 16–18C in late summer (Ojaveer and 2.0 Rotatoria others Lumberg, 1995). 3 – 1.5 Keratella spp. However, temperature was not a likely reason for the

m Synchaeta spp.

6 ﬀ ﬀ 1.0 observed spatial di erences in densities of di erent

10 ﬀ

× zooplankton groups. Di erences in salinity and in the 0.5 level of eutrophication between the archipelago and Ind ND ND ND 0.0 open sea stations are probably more important. The C-2 average Chl a concentration was the same as in the late 80 1980s, albeit typically higher than in other Finnish coastal waters (Pitka¨nen et al., 1993). The highest con- 3 60 – centrations were found in the eastern archipelago sta- 40 tions, which corresponds to the ﬁndings of Kauppila

mg C m 20 et al. (1995). The higher level of eutrophication may

ND ND ND have been one of the factors responsible for the 0 1 2 3 4 19 20 8 7 6 5 16 17 18 11 12 13 14 15 10 9 increased cilrate and rotifer biomass at the eastern stations. D-1 250 Top-down eﬀects may have modiﬁed the food web Ciliata others 3

– 200 Haptorina structure. By preying heavily on copepods at the eastern

m Oligotrichina Cercopagis

6 stations, might have an indirect positive 150 ﬀ

10 e ect on ciliates, which are regulated by mesozooplank-

× 100 ton predation in the Baltic Sea (Kivi et al., 1993; Uitto Ind 50 et al., 1995). A density of 1800 m 3 is very likely to ND ND ND 0 aﬀect the zooplankton community and, indeed, the D-2 140 biomass of copepods and cladocerans at station 15 was 120 3

– 100 80 60 Figure 7. Concentrations of various parameters by station mg C m 40 (arrows indicate archipelago stations; vertical lines separate 20 ND ND ND western from eastern stations; ND: no data). A. Chl a con- 0 centrations. B. Density (1) and biomass (2) of copepods 1 2 3 4 19 20 8 7 6 5 16 17 18 11 12 13 14 15 10 9 and cladocerans. C. Density (1) and biomass (2) of rotifers. Station no. D. Density (1) and biomass (2) of ciliates. 56 A. Uitto et al. the lowest observed. Avinski (1997) suggested that the Campbell, L., and Chowfraser, P. 1995. Differential effects of decrease in zooplankton density in the eastern Gulf of chemical preservatives and freezing on the length and dry weight of Daphnia and Diaptomus in an oligotrophic lake. Finland between 1994 and 1996 might have been caused 3 Archiv fu¨r Hydrobiologie, 134: 255–269. by predation by a Cercopagis population of 150 m . Carlton, J. T. 1989. Man’s role in changing the face of the We found an average density of 544 m 3 at the eastern ocean: biological invasions and implications for conservation stations, which was significantly higher than at the of near-shore environments. Conservation Biology, 3: 265– western ones (176 m3). The crustacean densities were 273. 3 ff Carlton, J. T. 1996. Pattern, process, and prediction in marine 21 000 and 35 000 m , but the di erence was not invasion ecology. Biological Conservation, 78: 97–106. significant. Owing to the patchiness of the horizontal Carlton, J. T., and Hodder, J. 1995. Biogeography and disper- and vertical distribution, predation effects are probably sal of coastal marine organisms: experimental studies on a also patchy, and losses in zooplankton biomass may be replica of a 16th-century sailing vessel. Marine Biology, 121: 721–730. compensated for from surrounding areas at relatively Cooper, S. D., and Coldman, C. R. 1980. Opossum shrimp short time scales. However, Cercopagis maybean (Mysis relicta) predation on zooplankton. Canadian Journal important zooplanktivore in the sheltered archipelago of Fisheries and Aquatic Sciences, 37: 909–919. areas, where the exchange of water masses is hindered by Edler, L. (ed.) 1979. Recommendations on methods for marine the topology (Pitka¨nen et al., 1993). biological studies in the Baltic Sea. Phytoplankton and chlorophyll. The Baltic Marine Biologists Publication, 5: According to Rudstam et al. (1994), mesozooplank- 1–38. ton in the northern Baltic Proper is controlled by Glamazda, V. V. 1971. On the occurrence of Cercopagic pengoi top-down predation by pelagic zooplanktivores (herring (Ostr.) in the Tsimlyansk Reservoir. Gidrobiologicheskij and mysid shrimps). Because of the similarity in the diet Zhurnal, 7: 70–71 (in Russian). Cercopagis Gorokhova, E. 1998. Zooplankton spatial distribution and of mysid shrimps, herring, and (Gorokhova, potential predation by invertebrate zooplanktivores. Second 1998), food competition may have increased. However, BASYS Annual Science Conference, 23-25.09.1998, this newcomer may also provide a new food link for Stockholm, Sweden. Paper Abstracts: 7. herring, if more food is available to the latter in the form Haapala, and Alenius 1994. Temperature and salinity statistics of Cercopagis biomass, than there would be if only for the northern Baltic Sea 1961–1990. Finnish Marine Research, 262: 51–121. indigenous metazooplankton were present. Neverthe- Hernroth, L. (ed.) 1985. Recommendations on methods for less, a dense Cercopagis population would still cause marine biological studies in the Baltic Sea. Mesozooplankton ‘‘leakage’’ of energy from the food web, because about Biomass Assessment. Baltic Marine Biologists Publication, 60% of the ingestion is lost in respiration and egestion in 10: 1–32. Hessen, D. 1990. Carbon, nitrogen, and phosphorus in Daphnia crustacean zooplankton. 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