© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Predation by herring (Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay
Department of Systems Ecology, Stockholm University SE-106 91 Stockholm, Sweden
*Correspondence to E. Gorokhova: tel.: +46 8 164256; fax: +46 8 158417. e-mail: elenag{at}system.ecology.su.se.
Cercopagis pengoi is a pelagic cladoceran that has recently colonized the Baltic Sea and the Laurentian Great Lakes and is recognized as a species with the potential to affect natural foodwebs. To study the consumption of C. pengoi by zooplanktivorous fish, stomach contents of herring (size range 52–252 mm) and sprat (57–116 mm) from a coastal area of the northern Baltic proper were examined in parallel with zooplankton samples. The overall proportion of fish preying on C. pengoi was high both for sprat (70%) and for herring (61%), and it accounted for 8 ± 23% and 20 ± 33% of prey dry weight in the diets. The predation on Cercopagis depends on its abundance and on fish size; herring showed a tendency to become more selective for Cercopagis with increasing size. The majority of diapause eggs found in sprat (69%) were immature and appeared digested, while this was the case only for 2% of the eggs found in herring. These results suggest that Cercopagis has become a significant component in the diet of zooplanktivorous fish and, therefore, its abundance may be controlled by fish predation.
Keywords: Cercopagis pengoi, diapausing eggs, diet, herring Clupea harengus, invasive species, predation, selectivity, sprat Sprattus sprattus
Received 21 August 2003; accepted 15 June 2004.
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Introduction |
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Cercopagis pengoi is a pelagic cladoceran that has recently colonized the Baltic Sea (Ojaveer and Lumberg, 1995; Uitto et al., 1999; Bielecka et al., 2000), including coastal waters of the Stockholm Archipelago (Gorokhova et al., 2000). Furthermore, the species has recently appeared in the Great Lakes (MacIsaac et al., 1999), where it is spreading rapidly (Therriault et al., 2002). The invasion has raised concerns that it may change the foodweb structure of native ecosystems (Vanderploeg et al., 2002). Indeed, when the closely related cercopagid Bythotrephes longimanus colonized North American lakes, it undoubtedly influenced these ecosystems (Yan et al., 2002). When established, Cercopagis may in a similar way affect resident zooplankton communities by selective predation, and this has recently been reported from the Gulf of Riga (Ojaveer et al., 1999) and Lake Ontario (Benoit et al., 2002). This may result in decreased grazing pressure on phytoplankton and enhanced algal blooms. Cercopagis may also impact fish populations by competing with 0-group fish for small prey, or conversely by becoming prey itself for older fish (Vanderploeg et al., 2002). Indeed, zooplanktivorous fish both in the Baltic and in the Great Lakes have been found to prey on Cercopagis when available (Ojaveer and Lumberg, 1995; Ojaveer et al., 1998; Antsulevich and Välipakka, 2000; Bushnoe et al., 2003). However, the extent to which fish consume C. pengoi may vary between size classes and species. Small fish may be unable to use it as prey due to gape size limitations, while large individuals may consume a significant proportion of Cercopagis production and even control its population development.
Herring (Clupea harengus L.) and sprat (Sprattus sprattus L.) are dominant species both in the commercial fishery and as zooplanktivores in the Baltic Sea. Before the invasion, their diets consisted mostly of calanoid copepods (Acartia spp., Eurytemora affinis, and Temora longicornis) and cladocerans (Bosmina coregoni maritima and Pleopsis polyphemoides), varying between the coastal and open sea areas and between northern and southern parts of the Baltic proper (Rudstam et al., 1992; Mehner and Heerkloss, 1994; Arrhenius, 1996; Antsulevich and Välipakka, 2000). After its appearance, Cercopagis has become a significant component in the diet of adult herring but not of the young-of-the-year (YOY) herring in Estonian and Finnish coastal waters (Ojaveer and Lumberg, 1995; Ojaveer et al., 1998; Antsulevich and Välipakka, 2000). These authors suggested that C. pengoi could improve herring feeding conditions and growth. However, the extent to which small fish consume C. pengoi has not been carefully examined and remains unclear.
The primary objective of this study was to estimate the contribution of C. pengoi to the diet of herring and sprat in a coastal area in the northern Baltic proper and to evaluate the selectivity for Cercopagis of different size classes of these fish species. In addition, we examined the frequency and condition of Cercopagis resting eggs in fish stomachs. The study was carried out during the summer 2002 in a deep (
30 m), enclosed bay (Himmerfjärden) located in the southern archipelago of Stockholm. This area was chosen because (1) the Cercopagis population is established in the area since at least 1997 (Gorokhova et al., 2000), (2) other coastal areas like this are most likely to become invaded by Cercopagis (Leppäkoski and Olenin, 2000), and (3) these habitats are nursery areas for many fish species, including herring (Axenrot, 2002).
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Material and methods |
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Zooplankton sampling and analyses
Zooplankton were sampled bi-weekly (July–October 2002, station indicated in Figure 1) from the bottom to the surface with a 90-µm WP-2 plankton net (
57 cm). On two occasions (3 August and 3 September), additional samples were taken in the upper 5–10 m with a 60-µm plankton net ( 23 cm). The samples were preserved and analysed according to the standard protocol of the Baltic Monitoring Programme (HELCOM, 1988). Dry weights of zooplankton were calculated according to Rosen (1981) and Hernroth (1985). When the dates for zooplankton sampling did not match the dates of fish sampling, zooplankton densities on the dates of fish sampling were obtained by linear interpolation between the abundances in the neighboring days.
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Cercopagis individuals were removed from the samples under a dissecting microscope prior to sub-sampling and processed separately. Conventional methods of population analysis of Cercopagidae were employed (Rivier, 1998); dry weights of Cercopagis were calculated according to Uitto et al. (1999).
Fish collection and stomach analysis
Fish were collected at three locations (Figure 1) on five occasions in July–September (Table 1). They were caught during night, in gillnets that were set 4–6 m below the surface. The nets were 3 m deep and had nine segments (each 2.5 m) with mesh sizes 5-, 6.25-, 8-, 10-, 12.5-, 15.5-, 19.5-, 24-, and 29-mm bar. Diet analyses focused on, but were not restricted to, fish from August and September, because Cercopagis was most abundant during this period. The collected fish were kept frozen (–18°C) until analysis; sometimes this resulted in deformed caudal fins, and as a measure of fish size, we used the distance (mm) from the tip of the nose to the base of the caudal fin. As a measure of the mouth size, we used the length (mm) of the lower jaw of the fish. A total of 106 herring and 80 sprat stomachs were analysed (64 empty; Table 1). When estimating the presence and condition of C. pengoi resting eggs, all non-empty stomachs were considered, while for the rest of the diet analysis, only those with 
8 identifiable objects were used (95 stomachs).
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The effect of fish size on dietary composition was examined by grouping fish into 50-mm size classes, with individuals larger than 200 mm forming the group ">200 mm" (Table 1). Herring <100 mm were mainly YOY fish produced from spawning in the study area (cf. Arrhenius and Hansson, 1996), while sprat in this size range were one-year-old fish. The stomach content was analysed using a dissecting microscope and an inverted microscope and identifying each prey item to the lowest possible taxonomic level. Cercopagis were recorded in two ways: (1) by weighing or (2) by counting the identifiable individuals or their body parts. The first method was used when the stomach contained a large bolus of individuals bundled together and the remnants of their bodies were relatively intact. Each bolus was transferred to a pre-weighed tin cup, dried at 60°C for 72 h, and weighed (±2 µg). The number of individuals in the bolus was calculated by assuming an individual dry weight of 20 µg (Uitto et al., 1999). It is possible that this underestimated the number of individuals, as some of them were partly digested, but we are confident that separating individuals (hundreds to thousands) and counting their remains would have introduced an even greater error. The second method was used when the remnants of Cercopagis were not aggregated and could be counted directly.
The number of Cercopagis resting eggs was determined from those visible in a bolus and those found free in the sample. Furthermore, the maturity of each egg was noted using the characteristics of Bythotrephes diapausing eggs (Jarnagin et al., 2000), i.e. amount of yolk present, coloration and thickness of the outer shell. The eggs were categorized as (1) mature – those with dispersed droplets, a bright-yellow coloration, thick and distinct shells and (2) immature – those which were clear or weakly colored on periphery, with very few or no droplets and thin outer shells.
Selectivity estimates and statistics
The selection of prey types was estimated using the Chesson (1983) selectivity index (
i); the index ranges from 0 to 1, corresponding to complete avoidance and full selection. In this study the three most abundant prey groups were considered, i.e. cladocerans (other than C. pengoi), copepods, and C. pengoi. As data on the in situ mysid abundance were unavailable, this prey was excluded from the selectivity estimates.
Using estimated i values, intra- and inter-specific differences in selectivity for Cercopagis were evaluated with a log-linear analysis (Upton, 1978). The analysis was based on a three-way frequency table with the dimensions: species (herring and sprat), length (longer or shorter than the median length, 97 mm), and position (i higher or lower than the median value for Cercopagis). Position was treated as a dependent variable, while species and length were independent variables. The number of fish that fit into a certain cell (e.g., herring x shorter than median length x i lower than median value; Table 2) is the frequency that is compared with the expected frequencies derived from the total number of observations and row/column sums.
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Results |
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Food availability
During the study period, Cercopagis densities were always low (<48 ind. m–3, Figure 2A), comprising <0.1% of the total zooplankton abundance and 0.4–1.2% of the biomass. Zooplankton were dominated by rotifers (Keratella cochlearis and Synchaeta spp., 19–80% of total zooplankton abundance) and copepods (mostly juvenile stages of Acartia bifilosa and Eurytemora affinis, 14–70%). Cladocerans (Bosmina coregoni maritima, Pleopsis polyphemoides, and Podon intermedius) contributed at most 10% to the total abundance, with usually less than 1–2% (Figure 2B). Cladocerans and copepods were abundant in June–July, decreasing during August, while the rotifers showed a very drastic decline during the mid-August (Figure 2B). Cercopagis was common from midsummer and showed a distinct peak on 10 September. The proportion of gametogenic females was also highest in this sample (16%, Figure 2A). Most of the gametogenic females (88%) had one-egg broods and hence we used a 1:1 ratio for egg:female, when using egg number to estimate the number of Cercopagis in a fish stomach.
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Stomach contents
Copepods (Acartia and Eurytemora) and cladocerans (mostly Bosmina) were dominant prey for sprat and the smallest of herring (Figure 3). Besides zooplankton, herring >114 mm had also eaten mysids (Neomysis integer) and small fish (data not shown). Irrespective of their size (herring of 52–252-mm length, sprat of 57–116-mm length), both fish species fed on Cercopagis and it occurred in 61% of the analysed herring and in 70% of the sprat. Herring stomachs contained up to 1299 and those of sprat – up to 116 C. pengoi. The proportion of Cercopagis in the diet was highest in 100–150-mm herring (Table 1, Figure 3), among which some fish had nothing but Cercopagis in their stomach. The higher proportion of Cercopagis in herring stomachs (Figure 3A) may at least in part be explained by their relatively larger mouth compared to that of sprat (Figure 4). Thus, although rare in the water column, Cercopagis contributed substantially to the stomach content of both fish species (Figure 3). The proportion of Cercopagis in diets increased with its abundance, with the strongest correlation derived for 100–150-mm herring (Pearson's r = 0.68, p < 0.003).
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Selectivity
There were statistically significant inter-specific differences in selectivity for Cercopagis between herring and sprat (Chesson selectivity index; Table 2). The difference was that the selectivity for Cercopagis increased with fish size for herring, but not in sprat.
Resting eggs
Resting eggs of Cercopagis were found in the stomachs of all size classes of the both species (Figure 5), sometimes in large quantities, e.g. 1299 eggs in a 113-mm herring. They were more frequent in herring than in sprat, with the highest frequency of eggs occurring (89%) in 100–150-mm herring (Figure 5A). Most of the eggs in sprat (69%) were immature (Figure 5B), while this was the case only for 2% of the eggs found in herring stomachs (6% if the stomach with 1299 eggs was excluded from the calculations). Most of the immature eggs found in sprat appeared as at least partially digested, with only thin empty outer shells containing essentially no yolk.
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Discussion |
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It has been suggested that Cercopagis will compete for herbivorous zooplankton with young stages of planktivorous fish, if these are unable to prey on Cercopagis due to its long caudal spine (Vanderploeg et al., 2002). In our study, however, fish down to a size of 52 mm fed on Cercopagis, including YOY herring. Despite its rarity in plankton (<1% of total zooplankton abundance and biomass), Cercopagis was ingested with high frequency by all fish <200 mm (Table 1). The predation on Cercopagis appears to depend on its abundance and to some extent on fish size; in particular, herring showed a tendency to become more selective for Cercopagis with increasing size. Thus, the colonization by Cercopagis has, at least in some areas, led to a shift in the feeding ecology of herring and sprat, the major zooplanktivores in the Baltic. Moreover, this shift occurs not only in adult herring (as suggested by Ojaveer et al., 1998), but also in sprat and in fish as young as metamorphosed YOY herring.
Cercopagis pengoi is present in the northern Baltic proper from July to October, being most abundant in August–September, i.e. at the same time of year as other zooplankton decline. This decline also occurred prior to the invasion of Cercopagis and is probably caused by factors such as resource availability or fish predation (Johansson et al., 1993; Adrian et al., 1999). Indeed, the consumption peak by fish occurs in August–September and the major zooplanktivores are YOY clupeoids (Rudstam et al., 1992; Arrhenius and Hansson, 1993). Therefore, as fish consumption increases and densities of native zooplankton decline, Cercopagis reaches its abundance peak and may become an important food source for zooplanktivorous fish during this period.
Like most cladocerans, C. pengoi is a cyclic parthenogen, and new population can be established from a single egg. The primary mode of reproduction is clonal, interspersed with periods (primarily in autumn) of sexual reproduction that involves formation of resting eggs (Rivier, 1998). It has also been suggested that resting eggs of Cercopagis can survive a passage through the fish digestive system (Antsulevich and Välipakka, 2000), and therefore fish could act as a dispersal vector. However, eggs carried by Instar I–III gametogenic females are in various stages of development when consumed by fish, and this may potentially affect the viability of those eggs following passage through the gut. We found a tendency in sprat, but not in herring, to ingest mostly females with immature eggs (Figure 5) and many of these eggs appeared partially digested. Because sprat has a smaller mouth compared to that of herring (Figure 4), it is possible that sprat feeds preferentially on smaller Instar I–II gametogenic females, which are more likely to have immature eggs, while herring selects larger Instar III females with dark, highly visible mature eggs as shown for many planktivorous fish and egg-carrying zooplankters. Jarnagin et al. (2000) showed experimentally that fully mature resting eggs of Bythotrephes survived the passage through the alimentary canal of yellow perch (Perca flavescens), while the hatching success of immature eggs was decreased. The impact of fish predation on the production of viable over-wintering eggs may therefore be influenced by the species composition of the zooplanktivorous fish and this may influence the recruitment of Cercopagis the following year.
Once invasive species are established, one of the few countermeasures that can be taken is to try to suppress the invader by managing its predators. This approach was taken in Lake Michigan, to control alewife and rainbow smelt (Rand and Stewart, 1998). The two dominant zooplanktivorous fish in the Baltic are herring and sprat, the populations of which are strongly influenced by the fishery and for which annual catch quotas are set by the International Baltic Sea Fisheries Commission. Our study shows that both these species are predators on Cercopagis and this may need to be accounted for in the management of the fishery, if we would like to reduce the abundance of Cercopagis. This would then be an excellent example of an application of the ecosystem-based approach to fisheries management, which is a cornerstone in the recently adopted common fisheries policy of the European Union (Anon., 2002). It should be acknowledged, however, that it is not fully understood to which extent herring, sprat and other zooplanktivores, like for example smelt (Osmerus eperlanus), jellyfish, and mysid shrimps, actually control Cercopagis through predation. Neither do we know if Cercopagis actually competes with the fish for prey or constitutes a new and important food web link to higher trophic levels.
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Acknowledgements |
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This research was supported by research grants from The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas) and Swedish Environmental Protection Agency. We thank B. Larsson for his invaluable help in collecting fish for analyses. We also thank M. Petersson (Ar Research Station, Gotland University, Sweden), L. Lundgren and B. Abrahamsson (Systems Ecology, Stockholm University, Sweden), and Karolina Eriksson-Gonzales (Linköping University, Sweden) for technical assistance and logistical support.
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