Review of western Baltic cod (Gadus morhua) recruitment dynamics

Transcription

1 ICES Journal of Marine Science (2011), 68(7), doi: /icesjms/fsr088 Review of western Baltic cod (Gadus morhua) recruitment dynamics Karin Hüssy National Institute of Aquatic Resources, Technical University of Denmark, Jaegersborg Alle 1, 2920 Charlottenlund, Denmark; tel: ; fax: ; Hüssy, K Review of western Baltic cod (Gadus morhua) recruitment dynamics. ICES Journal of Marine Science, 68: Received 26 December 2010; accepted 2 May Important processes in the recruitment dynamics of western Baltic cod (Gadus morhua) are identified. Spawning areas are in the deep, saline waters below m, depending on area topography. Spatial distribution remains relatively stable over time. Peak spawning shows an area-specific pattern, with progressively later spawning towards the east. Genetic stock structure and tagging indicate some degree of natal homing for spawning. The highly variable hydrodynamic conditions and the fact that cod eggs float in the water column cause their entrainment by currents, and their destination is determined by the prevailing winds and currents. Drift is almost exclusively to the east, but the magnitude and its impact on the structure of the affected stocks (Kattegat, western Baltic, and eastern Baltic) remains unresolved. Salinity limits the east west exchange of eggs as a consequence of the stocks differential requirement for neutral buoyancy. Superimposed on this, oxygen content and temperature have a significant effect on fertilization, egg/larva development, and survival. Within the Baltic Sea ecosystem, mixing of stocks may be anticipated and is particularly pronounced in the Arkona Basin because of its use for spawning by both western and eastern stocks, the advection of early life stages from the west and immigration/emigration from the east. Keywords: cod, migration, recruitment dynamics, stock interactions, western Baltic. Introduction The Baltic Sea is a large estuary with shallow connections to the ocean through the Danish Belt Sea. Freshwater inputs to the Baltic, m 3 s 21, and inflows of water high in salinity from the North Sea govern the hydrography of the region (Matthäus and Franck, 1992; Schinke and Matthäus, 1998). The inflow is driven by high air pressure associated with easterly winds over the Baltic that result in below-normal sea level caused by reduced precipitation and river run-off along with the advection of surface water masses to the west followed by longer periods (several weeks) of zonal winds (from the west) over the North Atlantic and Europe, with only small fluctuations in direction (Matthäus and Franck, 1992; Schinke and Matthäus, 1998). Salinity and temperature stratification vary significantly horizontally, salinities being lower north and east and higher west and south. A seasonal thermocline develops in spring as a result of surface heating, and it is maintained by solar input until autumn. As a result, the hydrodynamic conditions within the Baltic Sea are extremely variable, particularly in the narrow Belt Sea, the Sound, and the Fehmarn Belt, through which all water passes in and out of the eastern Baltic Sea (EB; Matthäus and Franck, 1992; Schinke and Matthäus, 1998). The Baltic Sea has been partitioned into Subdivisions (SD) by ICES (Figure 1), depending on prevailing geographic and hydrological conditions. SDs encompass the EB, SDs the western Baltic Sea (WB), and SD 21 the Kattegat. Traditionally, cod (Gadus morhua) in the Baltic Sea have been considered to be two separate stocks, one east of the island of Bornholm, the other from west of Bornholm to the Sound and the Danish Belts (Bagge et al., 1994). Baltic cod populations are assessed and managed as two distinct stocks, EB cod in SDs and WB cod in SDs 22 24, and fish are assigned to stock depending on the management area in which they were caught. A third stock of importance to the study is the Kattegat cod in SD 21. However, a substantial body of literature suggests that stock dynamics are more complex than this. For the short-term predictions used in stock assessment, early and precise estimates of recruitment are essential. In heavily fished stocks like WB cod, where the age structure is dominated by a few age groups and with a high contribution of first-time spawners, such predictions are of basic importance. As is obvious from time-series of spawning-stock biomass (SSB) and recruitment (R), the WB cod stock has fluctuated considerably during the past 40 years (Figure 2a). Moreover, recruitment success (recruitment per unit spawning biomass) also changed markedly (Figure 2b), indicating either that SSB is not an adequate measure of reproductive success or that environmental conditions and potential species interactions influence recruitment. To make any predictions about recruitment, it is necessary to consider all steps of the life cycle: stock origin of the recruits (distribution and migration of parents), stock structure (mean age and mean size of spawning fish), origin (spawning areas and time), number spawned (stock composition, maturation, and fecundity), destination (drift of early life stages), and factors limiting the survival of larvae (environmental factors, predation, human influence). Detailed reviews of the EB stock in SDs already exist (Bagge et al., 1994; ICES, 1994, 2005; CORE, 1997; Vallin et al., # 2011 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. 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2 1460 K. Hüssy Figure 1. Map of the Kattegat and Baltic Sea area showing ICES Subdivisions (numbers) and management areas (Kattegat; western Baltic Sea, WB; and eastern Baltic Sea, EB) enclosed by bold lines. 1999; STORE, 2002). This review on recruitment processes therefore aims at summarizing existing knowledge of cod ecology in the WB stock in SDs 22 24, primarily covering research over the past three decades, to provide a basis for future management and to predict the impact of changes in environmental conditions caused by natural and anthropogenic activities. Conditions observed in the stocks of the EB and Kattegat that may be relevant for WB cod are included in the review. Reliable information on stock distribution, spawning areas and times, adult maturation, and fecundity, as well as the processes influencing the growth and survival of early life stages and the impact of these parameters on recruitment of the WB cod, are summarized. Adult stock distribution and migration In general, cod are distributed throughout the WB from shallow to deep water, with a tendency towards greater depth occupation during winter (Thurow, 1970; Oeberst, 2008). A detailed map of the distribution of WB cod is given in Figure 3. As part of their seasonal cycle, adult cod undertake distinct and highly complex migrations after the onset of maturation, targeting specific feeding and spawning areas (Aro, 1989). These migrations between their feeding and spawning grounds are extensive and variable between areas in the WB (Otterlind, 1985). The general direction of the spawning migrations in the Belt Sea is towards the southern Kattegat and Danish Belts (Bagge, 1969; Otterlind, 1985), whereas cod tagged in Mecklenburg Bay initially disperse eastwards along the German/Polish Coast. After 6 17 months, they either are back in Mecklenburg Bay or have moved in apparent feeding migrations towards Møn (Berner, 1967, 1971a). In early winter, these fish move towards Kiel Bay, Little Belt, and particularly Great Belt and the southern Kattegat to spawn (Berner, 1967). There seem to be considerable interannual differences in the strength and direction of these migrations (Bagge, 1969). Cod in the eastern part of the WB, specifically the Arkona Basin, follow a quite different migration pattern. Small fish generally seem to be rather stationary, suggesting that adult migrations are probably associated with spawning (Berner, 1967, 1974). Adult cod tagged in the Arkona Basin migrate both west and east, even east of the Bornholm Basin (Berner, 1967, 1971b; Otterlind, 1985). Emigration has also been observed towards the Kattegat, mainly through the Belts and not the Sound (Otterlind, 1985). The strength of these migrations appears to vary between years. Nevertheless, there seems to be a geographic pattern in that most cod from the eastern Arkona Basin move into the Bornholm Basin (to spawn), whereas fish from the western Arkona Basin migrate east of Bornholm to a lesser extent, their main destination being towards the Belt Sea (Otterlind, 1985). Otterlind (1985) hypothesized that the direction of the spawning migrations of WB cod in the Arkona Basin depends on environmental conditions in the area, mainly salinity, before spawning. A different explanation is offered by Berner and Borrmann (1985), who noted that cod tagged from January to April moved west, that those tagged from May to August moved east, and that those tagged from September to December tended to stay in the Arkona Basin. These migrations may, therefore, not only be attributable to hydrographic conditions, but may indicate contributions of spawning components of both EB and WB stocks in the Arkona Basin. Translocation experiments showed that cod transported from the Kattegat to the Åland Islands, eastern Bornholm, and the Sound, or in the opposite direction, did not return to their origin (Otterlind, 1965, 1985; Bagge, 1983). Contrary to this, cod from the Swedish Kattegat coast returned to the North Sea during the spawning season (Svedäng et al., 2007). It remains unclear whether this inability for natal homing in Baltic cod represents true conditions or is the result of the translocation. Cod translocated within the Bornholm/Arkona area, however, did seem to find their way home. They also showed approximately the same distribution pattern as natal cod, indicating that distribution patterns are in response to prevailing hydrographic conditions. Several other studies support this hypothesis of separation between stocks, with some mixing in the Arkona Basin. For example, the number of fin rays in the first and second dorsal fins has been used as a phenotypic marker to evaluate stock identity (Schmidt, 1930; Poulsen, 1931; Kändler, 1949a; Birjukov, 1969; Berner and Vaske, 1985). Müller (2002) found differences between EB cod and stocks west of Bornholm, with mixing in the Arkona Basin. Similar results have been obtained with other markers, such as body height, otolith size, head characteristics, and length weight ratios (Berner and Vaske, 1985; Berner and Müller, 1989, 1990). Nielsen et al. (2003) used genetic differentiation to evaluate the spatial separation of different cod stocks. They found high levels of differentiation in the transition zone between stocks of the North Sea and the EB. SD 24 is the centre of transition between the two types. In all samples from the transition area, intermediate genotypes were found, indicating admixture of different populations. In other words, in the Arkona Basin, cod do not merely migrate across management borders, but some fraction of EB and WB stocks actually interbreed. Adding to this interbreeding may be the advection of early life stages (discussed below). Throughout the North Sea and Baltic Sea, juvenile cod are genetically related to the adults in the same area (Nielsen et al., 2005), but one exception is that WB juvenile cod from the Arkona Basin are more closely related to the spawning population in the Belt Sea than to adults from the Arkona Basin.

3 Western Baltic cod recruitment dynamics 1461 Figure 2. Stock parameters of the WB cod stock over the years : (a) SSB (t, grey columns) and recruitment, shifted back 1 year to represent year-class strength (thousands, black line and circles) and (b) recruits (shifted back 1 year to represent year-class strength) produced per unit of spawning stock (R/SSB). In summary, within the WB, mixing of WB and EB cod stocks may be anticipated to result from migrations of adult fish, causing mixing that is particularly pronounced in the Arkona Basin. Spawning areas Identification of spawning grounds is often based on ichthyoplankton surveys, where the densest areas of egg distribution are assumed to be where the adults spawn. There are two major problems with this approach. First, egg distribution does not necessarily reflect the spawning areas, because egg buoyancy may cause cod eggs to sink to greater depth if the salinity is low. In this case, quantitative sampling is difficult, because it is impossible to sample close to the seabed near the greatest concentrations of eggs. Second, in a hydrographically highly variable environment such as the WB, with current speeds up to 20 cm s 21, the distributions of eggs and early larvae are influenced by the prevailing current and may easily, within a few days, be entrained far from their spawning origin. Hence, identification of spawning areas from the results of ichthyoplankton surveys may lead to erroneous conclusions. Validation by comparing with the distribution of running adults is necessary. The various areas are dealt with separately in terms of spawning importance below, but to summarize, spawning areas within the Kattegat and WB appear to be located mainly in the deep, saline waters of specific areas, summarized in Figure 4. The Arkona Basin seems to be used as a spawning ground by both the WB and EB cod stocks.

4 1462 K. Hüssy Figure 3. Map showing all relevant localities in the western Baltic Sea. Isobaths correspond to 20-m depth intervals. Figure 4. Spawning areas (black) in the Baltic Sea from the Kattegat to the Bornholm Basin derived from a combination of ichthyoplankton surveys and surveys of spawning adults. Kattegat and Sound In recent years, two areas in the southeastern Kattegat appear to have been important for the reproduction of cod, just north of the entrance to the Sound and off the coast at Falkenberg, Sweden (Vitale et al., 2008). These spawning grounds were identified by sampling running adults and are in agreement with reported spawning aggregations from earlier periods (Svedäng and Bardon, 2003). Ichthyoplankton surveys have confirmed this pattern (Hagstrøm et al., 1990), but have also shown additional spawning in the deeper parts of the southwestern Kattegat (Hagstrøm et al., 1990). Whether these areas actually represent spawning areas or are the results of current-related entrainment of early life stages remains unresolved. Because of the currently low SSB, some of the traditional, but minor, spawning areas in

5 Western Baltic cod recruitment dynamics 1463 the central and northern Kattegat and in the bays of Skälderviken and Laholmsbukten (Sweden) may have disappeared (Svedäng and Bardon, 2003; Vitale et al., 2008). Little and Great Belts Only limited information is available on the importance of the Danish Belts as spawning areas. Tagging results from adult cod indicate that the Great Belt and southern Kattegat is used for spawning by fish from the Belt Sea near Bagenkop, Denmark (Bagge, 1969), as well as by cod from Mecklenburg Bay (Berner, 1967). Also, the Little Belt supports a considerable spawning component (Thurow, 1970). Kiel Bay, Fehmarn Belt, and Mecklenburg Bay The earliest systematic mapping of cod spawning in the WB was by Kändler (1949a, b, 1950) and Müller (1988). Ichthyoplankton surveys of high spatial and temporal resolution demonstrated spawning in Kiel Bay, Mecklenburg Bay, and the Arkona Basin (Kändler, 1950). Eggs were most abundant in the centre of the WB, particularly south southwest of Langeland and northwest of Fehmarn, with considerable interannual variability in abundance (von Westernhagen et al., 1988). Spawning activity seemed to be limited in Mecklenburg Bay (von Westernhagen et al., 1988) and restricted to depths.20 m (Bleil and Oeberst, 2000, 2002), perhaps indicative of real differences in reproductive output, but also possibly attributable to sampling time in relation to peak spawning. The latter is a common problem if sampling is only once per year. Mapping spawning adults in Kiel Bay with equal spatiotemporal resolution, Thurow (1970) identified Süderfahrt/ Millionenviertel and Dorschmulde/Vejsnäs Trough as important spawning areas, whereas the Hohwachter Bucht and Stollergrund shoal were not important (Figure 3). The distribution of these spawning areas corresponds closely with ichthyoplankton-derived areas. In contrast to Kändler (1950) and Müller (1988), Thurow (1970) found that sampling stations within the Fehmarn Belt and Mecklenburg Bay only contained few spawning cod, suggesting that the high densities of eggs in the area did not originate from spawning activities actually in the Belt. In Mecklenburg Bay, spawning seemed to be even more restricted and limited to an area north northwest of Kühlungsborn. Its existence as a spawning area has been confirmed by trawl surveys recently (Bleil and Oeberst, 2000, 2002). Extensive tagging programmes support the hypothesis that adult cod use Mecklenburg Bay mainly to feed and migrate through the Fehmarn Belt to the main spawning areas in Kiel Bay (Berner, 1967, 1968). Arkona Basin The deep portions of the Arkona Basin.40 m deep are considered to be where WB cod spawn (Bleil and Oeberst, 2000, 2002). Information on the timing of spawning activities (Bleil and Oeberst, 2004; Bleil et al., 2009), as well as migration patterns based on tagging studies (Otterlind, 1985), suggest that the Arkona Basin may be an area used for spawning by both EB and WB cod stocks. The area may be of importance also for recruitment of EB cod (Bleil and Oeberst, 2004; Bleil et al., 2009). Spawning time Throughout the distribution of cod stocks in the Kattegat/Baltic Sea, the progression of the spawning season follows similar patterns. The whole spawning season for all stocks lasts for 6 7 months, but peak spawning is restricted to 1 2 months (Kändler, 1949b; Thurow, 1970; Bleil and Oeberst, 1997, 2004; Wieland et al., 2000; Vitale et al., 2008; Bleil et al., 2009). In all stocks, there is a pronounced size effect, large females arriving at the spawning grounds before smaller ones, producing more batches, and therefore spawning longest (Thurow, 1970; Bleil and Oeberst, 1997, 1998, 2004; Tomkiewicz et al., 2003; Bleil et al., 2009). This seems to be an endogenously controlled feature of the maturation cycle, because cod in captivity exhibit the same spawning patterns (Bleil and Oeberst, 1998). EB males seem to follow a much less pronounced size-dependent timing than females (Tomkiewicz and Köster, 1999), whereas there is no size effect in WB males (Bleil and Oeberst, 1997). The spawning components differ in their timing of peak spawning, with a pronounced trend towards progressively later spawning along a gradient from northwest to east (Bleil and Oeberst, 1997; Bleil et al., 2009). The earliest comparative studies of egg distributions in relation to area (Kiel Bay, Mecklenburg Bay, Arkona, Bornholm, and Gotland basins, and Gdánsk Deep) revealed a pronounced eastward delay in both peak spawning time and a prolongation of the spawning season (Kändler, 1949b). Cod in the Kattegat and Sound are the first to commence spawning, peaking in January/February (Vitale et al., 2005), followed by cod in Kiel Bay and Mecklenburg Bay in March/April (Bleil and Oeberst, 2004; Bleil et al., 2009). In the Arkona Basin, spawning peaks in May/June, but there is considerable overlap with the Belt Sea and also with Bornholm Basin cod that peak in July/August (Wieland et al., 2000; Bleil et al., 2009). In the Arkona Basin, the spawning season is the longest of all, supporting the belief that the area may actually be a spawning ground for both WB and EB cod stocks (Bleil and Oeberst, 2004). Back-calculation of hatching dates from juveniles supports this hypothesis (Oeberst and Böttcher, 1998). The ranges and peaks of the spawning seasons of the different stocks are summarized in Table 1. Considerable interannual variations in peak spawning have been reported from Kiel Bay, based on ichthyoplankton samples, changing from February to April in consecutive years (Müller, 1988). The abundance of cod eggs in the Fehmarn Belt is similarly variable between years (Kändler, 1950), and it appears to be influenced strongly by winter water temperature. Warmer water leads to earlier spawning and a shorter spawning season than cooler water, in which the time from first spawning to the peak, and the duration of the entire season, is longer (Kändler, 1950). Another factor that may influence spawning time is salinity, in that suboptimal salinity leads to a cessation of spawning in the laboratory (Bleil, 1995) and apparently also in the wild (Kändler, 1950). Studies of adults with running gonads that support these interannual variations unfortunately do not exist despite large sample sizes for certain time-series (Bleil et al., 2009). To summarize, spawning begins in January/February in the Kattegat/Sound, with a progressive delay towards the east, ending in July/August in the Bornholm Basin. There are indications that the Arkona Basin may be used by both WB and EB cod for spawning. Peak spawning seems to be influenced by temperature, with later and more prolonged spawning in cooler years, and may vary by up to 2 months. Sexual maturation and fecundity Overall, recruitment in the WB cod stock seems to be linked to stock fecundity, particularly the proportion and condition of

6 1464 K. Hüssy Table 1. Spawning season of individual cod stocks, listing the time of peak spawning, and references to sampling. Area Spawning season Peak spawning Years Method Reference Kattegat September May January/February 2002/2003 Histology a Vitale et al. (2005) Sound November May January/February 2002/2003 Histology Vitale et al. (2005) Kiel Bay January June February/March Plankton b Kändler (1949b) January June March Adults c Thurow (1970) December July March/April 1970/1971 Plankton Müller (1988) February May March/April Adults Bleil et al. (2009) Mecklenburg February May April Plankton Kändler (1949b) February June March/April Adults Bleil et al. (2009) Arkona February August February/April Plankton Kändler (1949b) March September June/July Adults Bleil et al. (2009) Bornholm March October July/August Plankton Kändler (1949b) March June May/June Plankton Wieland et al. (2000) March November July/August Plankton Wieland et al. (2000) February November July/August Adults Bleil et al. (2009) March September July Adults Tomkiewicz and Köster (1999) Gdánsk March October August Plankton Kändler (1949b) Gotland April August May Plankton Kändler (1949b) a Histology, histology of gonads. b Plankton, ichthyoplankton surveys. c Adults, survey of adult maturity. female spawners. Earlier maturation and greater egg production, in general and especially in larger females, may influence reproductive success positively, as outlined below. Maturation Regardless of stock, males generally mature younger and smaller than females, varying by 10 cm in length at 50% maturity. Females generally dominate with increasing size and age in both WB (Thurow, 1970; Bleil and Oeberst, 1997, 2004; Bleil et al., 2009) and EB cod (Bleil and Oeberst, 1997, 2004; Tomkiewicz et al., 1997, 2003; Bleil et al., 2009). This leads to a skewed sex ratio, which, contrary to the EB (Tomkiewicz and Köster, 1999), seems to persist throughout the spawning season (Thurow, 1970; Berner, 1985). Reasons for the skewed sex ratio in spawning aggregations of older cod are that males participate in spawning activity younger and arrive earlier and stay longer on the spawning grounds than females (Thurow, 1970; Bleil and Oeberst, 1997, 2004; Tomkiewicz et al., 2003; Bleil et al., 2009). This exposes males to a prolonged period of intense fishing pressure (Thurow, 1970; Tomkiewicz et al., 1997). Also, physical condition after spawning decreases more in males than in females, probably because of the prolonged reduced food consumption during spawning, which further increases male mortality (Thurow, 1970). There are regional differences in sexual maturation patterns, in that the size at sexual maturation decreases progressively from west to east by 5 cm(thurow, 1970; Bleil and Oeberst, 1997, 2004; Tomkiewicz et al., 1997; Bleil et al., 2009), but with variations between years. Fecundity Absolute fecundity (the total number of eggs produced during a spawning season by a female) increases with fish size in all stocks (Schopka, 1971; Bleil and Oeberst, 1996; Kraus et al., 2000). There are pronounced year effects in both absolute and relative fecundity (total number of eggs produced per gramme female body weight; Berner, 1985; Bleil and Oeberst, 1996; Kraus et al., 2000). These short-term variations are superimposed on long-term changes that have prevailed over the past few decades. In the 1980s, individual fecundity in EB cod was considerably higher than in the mid-1950s (Berner, 1985). In the 1990s, fecundity increased in the EB (Kraus et al., 2000), whereas fecundity in WB cod, particularly large females, was stable (Bleil and Oeberst, 2005). Concurrently, there were changes in egg weight, with increasing egg weight in WB cod and decreasing weight in EB cod, presumably as a consequence of limited space in the ovaries (Bleil and Oeberst, 2005). All these authors suggest that decreased density-dependent competition leads to higher fecundity in EB cod at the expense of a smaller egg size. A direct consequence of this would be a decrease in egg buoyancy, with ensuing increased egg mortality for EB cod, whereas the eggs produced by WB cod would have increased buoyancy, which would be beneficial especially on the Arkona Basin spawning ground, as discussed below. The positive impact of fish condition, mediated by food availability, on fecundity is well known for a range of cod stocks (Marshall et al., 1998, 2003; Marteinsdottir and Steinarsson, 1998; Kraus et al., 2000; Lambert and Dutil, 2000; Sherwood et al., 2007). The WB cod stock is no exception, because the abundance of recruits, at least within short periods, seems to be correlated with stock fecundity and the proportion of female spawners (Oeberst and Bleil, 2003), but this does not appear to explain the variations observed in recruits per SSB (R/SSB; Figure 2b). Survival of early life stages The production of viable eggs is the basis of a fish stock s recruitment potential, and knowledge of the variables influencing the survival of early life stages is essential (von Westernhagen, 1970; Bleil, 1995; Vallin et al., 1999). What follows in the sections below, therefore, is a review of specific environmental factors that affect egg development and survival. Environmental factors Overall, because of the salinity requirements for spermatozoa activity and egg buoyancy, EB cod can spawn successfully and their eggs survive in the WB. However, WB cod cannot reproduce

7 Western Baltic cod recruitment dynamics 1465 Table 2. Critical values of parameters in egg fertilization and early life-stage development for different cod stocks in the Baltic Sea. Stock Parameter Critical value Reference Kattegat Neutral egg buoyancy psu Nissling and Westin (1997) Sound Neutral egg buoyancy psu Nissling and Westin (1997) Neutral egg buoyancy psu Westerberg (1994) Egg size (floating eggs) February 1.44 mm Westerberg (1994) March 1.40 mm Westerberg (1994) Egg vertical distribution (sill) 1 4 m, max. at 2.5 m Westerberg (1994) Mean egg density (sill) 17 eggs 100 m 23 Westerberg (1994) Egg vertical distribution (Ven) m, max. at 12 m Westerberg (1994) Mean egg density (Ven) 35 eggs 100 m 23 Westerberg (1994) Larvae vertical distribution psu, m Westerberg (1994) Belt Sea Spermatozoa activation psu Nissling and Westin (1997) Neutral egg buoyancy psu Nissling and Westin (1997) Western Baltic Maximum egg concentration in field.17.6 von Westernhagen et al. (1988) Total egg mortality 96 99% von Westernhagen et al. (1988) Fehmarn Egg hatching Optimum 4 88C von Westernhagen (1970) Egg hatching Optimum psu von Westernhagen (1970) Mecklenburg Egg hatching Optimum C Bleil (1995) Arkona Neutral egg buoyancy psu Nissling and Westin (1997) Bornholm Spermatozoa activation psu Nissling and Westin (1997) Neutral egg buoyancy psu Nissling and Westin (1997) Egg hatching Optimum 2 108C Petereit et al. (2004); Wieland and Jarre-Teichmann (1997) Egg survival, O 2 at incubation,2mll 21 : none Wieland et al. (1994); Rohlf (1999),5mll 1 : declining Köster et al. (2005) Larval activity,5mll 21 : declining Rohlf (1999) Gotland Neutral egg buoyancy psu Nissling and Westin (1997) All stocks Incubation time (d) e temp Page and Frank (1989); Thompson and Riley (1981); Wieland et al. (1994); von Westernhagen (1970) successfully in the Bornholm Basin, because of the low oxygen content there at the depth to which WB eggs sink. This has implications for stock dynamics, in that mixing of stocks (e.g. successful spawning) is possible in the WB spawning areas, where salinity is often high enough for both stocks. Superimposed on this primary driver, oxygen content and temperature have a significant effect on egg/larva development and survival. The critical values are summarized in Table 2. Salinity The Baltic Sea is the world s largest brackish-water sea, and cod, being a saltwater species, are at the limit of their geographic distribution. Low salinity may limit fertilization by inhibiting the activation of spermatozoa. The minimum salinity required differs between stocks: psu in EB cod and psu in WB cod (Nissling et al., 1994; Nissling and Westin, 1997). Laboratory experiments have revealed such differences also at the egg stage, with average salinity at neutral buoyancy of 14.5 psu in EB cod and psu in WB cod (Nissling and Westin, 1997). At lower salinity, eggs will sink and fail to develop to hatching (von Westernhagen, 1970). Translocation experiments have shown that translocation between marine and brackish conditions does not influence spermatozoa salinity requirements in either adult EB cod kept at the environmental salinity of WB cod or adult WB cod kept at the salinity of EB cod (Nissling and Westin, 1997). This means that spermatozoa of an EB cod kept at high salinity (as in the WB) could still fertilize eggs at the same low salinity. Neutral egg buoyancy only changed marginally to psu in EB cod and decreased to psu in WB cod. Therefore, transfer of individual cod to different conditions leads to minor adaptation, but in essence, the traits remain the same, suggesting that they are genetically determined. Ichthyoplankton surveys confirm these critical salinity limits. In the Kattegat, south of Ven, and in the Sound, cod eggs are found at salinities of psu, corresponding to depths of and 1 4 m, respectively, with maxima at 12 and 2.5 m, respectively (Westerberg, 1994). In Kiel Bay, highest concentrations of eggs are at 17.6 psu, suggesting that salinity limits the eastward distribution of eggs originating from Kiel Bay as they sink to the seabed and die, explaining the lesser abundance of eggs farther east (von Westernhagen et al., 1988). That egg mortality may be related to physical damage to the eggs when they come into contact with the sediment. For eggs transported to the Bornholm Basin, survival is limited by a lack of sufficient oxygen at the depth to which the heavier WB eggs sink (Nissling et al., 1994). Von Westernhagen et al. (1988) also associated increasing deformities in cod embryos from Little Belt to Kiel Bay and Mecklenburg Bay with decreasing salinity (possibly interacting with oxygen, temperature, and pollutants). Deformation rates varied between 18 and 32%, with greatest malfunction in the youngest eggs, presumably because they died before they could be sampled at an older age. Temperature Temperature is one of the strongest parameters affecting the metabolism of an individual fish directly and mortality indirectly by determining the development time from fertilization to hatch,

8 1466 K. Hüssy from hatch to first-feeding, and from first-feeding to becoming an established feeding larva. Regardless of stock, geographic distribution, and female contribution, egg development time appears to follow a negative exponential pattern (Table 2; von Westernhagen, 1970; Thompson and Riley, 1981; Page and Frank, 1989; Wieland et al., 1994; Petereit et al., 2004). However, all these studies were based on few parent fish and showed substantial individual variation (von Westernhagen, 1970; Wieland et al., 1994). The experimental designs may have introduced bias in the form of female- and batch-number effects. Therefore, whether differences between studies are attributable to stock-specific differences in temperature response of egg development or to the influence of individual variation and the experimental design used remains unclear. Although cod eggs develop at a wide range of temperature, egg mortality indicates that there is a range within which survival is greatest. The range for successful hatching for WB cod from Mecklenburg Bay is C, with an optimum at C (Bleil, 1995); for the Fehmarn Belt, the range is 4 88C (von Westernhagen, 1970). At suboptimal conditions, egg mortality increases because of less survival and more deformities (von Westernhagen, 1970). However, these temperature ranges may be affected by salinity, because a pronounced cross-effect causes eggs to tolerate lower salinity if temperatures are low (von Westernhagen, 1970). In EB cod, egg survival is also reported to be influenced negatively at temperatures,28c (Wieland and Jarre-Teichmann, 1997) and.108c (Petereit et al., 2004), with extreme temperature conditions also affecting larval size at hatching negatively (Petereit et al., 2004). Oxygen Development, growth, activity, and the reproduction of most living organisms are based on respiration. If not provided with sufficient levels of oxygen, an organism will die, and cod eggs are no exception. In EB cod, survival drops sharply at oxygen concentrations,5 mll 21, and no eggs survive concentrations,2 mll 21 (Wieland et al., 1994). Lower oxygen concentrations are apparently tolerated better at lower temperatures (Wieland et al., 1994). Using experimental data from Wieland et al. (1994) and Rohlf (1999), Köster et al. (2005) described the viable hatching of cod eggs at different levels of oxygen concentration during egg incubation adjusted to survival at normoxic conditions. The development time to hatching, on the other hand, does not appear to be affected by oxygen concentration, if concentrations are sufficiently high to ensure egg survival (Wieland et al., 1994). What is affected is the activity level of the larva, which is lower at low oxygen incubation (Rohlf, 1999). No such information exists for the WB, but it can be assumed to be similar, based on almost identical relationships in other stocks (Alderdice and Forrester, 1971). Therefore, a combination of salinity, temperature, and oxygen concentration may determine egg and, to a certain extent, larva survival in the WB (Kändler and Wattenberg, 1939; Kändler, 1944, 1960). Drift Hydrodynamic conditions, particularly within the narrow Belt Sea, the Sound, and the Fehmarn Belt, are extremely variable (Matthäus and Franck, 1992; Schinke and Matthäus, 1998). The German bays and the Arkona Basin are also highly dynamic because of their limited water depth. Current speeds of up to 18 cm s 21 have been recorded in the Fehmarn Belt (Matthäus and Franck, 1992). As cod eggs float in the water column, they are entrained by such currents, and their destination is determined by the prevailing winds and currents. In the sections following, different observations and attempts to quantify the magnitude of this drift are summarized. Overall, there is potential for considerable mixing of stock components in the Baltic Sea ecosystem, with drift of early life stages one of the potential key drivers for recruitment and stock mixing. Drift depends on wind-driven current speeds and directions and is almost exclusively eastwards, but there is a wide range of variables that can modulate the impact of this drift, e.g. salinity, which limits the east west exchange of eggs through the differential salinity requirements of the two stocks preventing eggs from sinking to the seabed. Regression studies Several studies have examined the correlations between stock parameters and environmental factors with recruitment in different areas of the Baltic. Although the studies do not address drift directly, the variables examined can be regarded as indicators for entrainment processes. Therefore, recruitment in SD 22 has been correlated with bottom temperature (and, to some extent, salinity) and with recruitment in SD 21 (Kattegat; Müller et al., 1988). In SDs (and, to some extent, SD 21), recruitment has been correlated with SSB in SDs and oxygen content during the spawning season (Berner and Müller, 1988; Müller, 1994). Notwithstanding, recruitment fluctuated more in SD 22 than in SD 24, and the indices were not correlated (Müller, 1994). In the Arkona Basin (SD 24), recruitment was positively correlated with bottom salinity and recruitment in the EB (Berner et al., 1988). These studies show the importance of hydrographic conditions, the advection of larvae from neighbouring stocks, and the complexity of recruitment dynamics in the area. The general trend of early life-stage drift appears to be from the Kattegat and the Belt Sea towards the Arkona Basin and the EB. In the Arkona Basin, however, the correlation with recruitment in SDs suggests an influx of early life stages from the EB. This entrainment must take place during the late larva stage, because the vertical distribution of eggs and early larvae prevent them from being advected towards the west (Hinrichsen et al., 2001a, 2003a). Length and age frequencies To evaluate the extent of transport/migration between different stock components, another approach is to use length and age frequencies and derived hatching dates (Oeberst and Böttcher, 1998). Based on these hatching dates and the length distributions of juveniles caught on surveys, the estimated proportion of WB cod among age 1 fish in the Bornholm Basin (from 1992 to 1996) was estimated at 10 90%, and as much as 15 75% at ages 2 and 3 (Oeberst, 2000, 2001), with lower proportions in strong year classes. Concurrently, substantial migrations from the EB to the Belt Sea were proposed where age 1 fish contributed as much as 48% (in 1995) to the entire stock. Ichthyoplankton observations In the Sound, most eggs float in the halocline (Westerberg, 1994). During inflow events, the depth of the halocline decreases, and eggs are entrained across the sills towards the Arkona Basin. Because of the concentration in the halocline, even small inflows may result in extensive transport of eggs. The estimated egg flux across the sill amounted to eggs year 21 (in 1993 and 1994), some 10 30% of the eggs produced. Westerberg (1994)

9 Western Baltic cod recruitment dynamics 1467 hypothesized that the eggs are entrained towards the Arkona Basin and may end up in the Bornholm Basin, which could be a mechanism for supplementing the EB cod stock during recruitment failure. However, this hypothesis does not consider the stockspecific salinity requirements for neutral egg buoyancy discussed above. Eastward transport will cause WB cod eggs to sink to the seabed, preventing their survival. Moreover, recruitment failure in the EB stock is linked to stagnation in deep water because of a lack of inflow (Köster et al., 2005), in which case there is also limited entrainment of eggs from the WB. The impact of current direction and speed on larvae is more complex, because larvae in the WB only seem to be found shallower than m (Klenz, 1999). With this distribution mainly in surface waters, their drift destination would be influenced strongly by the prevailing winds, as the capture of juveniles in the Fehmarn Belt has demonstrated (Bauer et al., 2010). Unfortunately, there is hardly any information available on the vertical distribution of cod larvae in the WB, presumably because of the limited numbers captured during surveys. Drift modelling A useful tool for studying the impact of early life-stage entrainment is hydrodynamic modelling (Hinrichsen et al., 1997). The model in use is three-dimensional and eddy-resolving, and it includes data-assimilation techniques that use temperature and salinity data from monthly hydrographic surveys and supports the use of Lagrangian particle-tracking techniques (Lehmann, 1995). The flowfields are driven by atmospheric forcing, with data obtained from the EUROPA Model of the German Weather Service (Deutscher Wetterdienst, Offenbach). In the EB, this modelling approach has been used to study the distribution and drift of early life stages (Hinrichsen et al., 2003a), the impact thereof on the survival of larvae (Hinrichsen et al., 2001b, 2003b), and the influence of copepod species composition on the growth and survival of larvae (Hinrichsen et al., 2002). For the WB, only one such study has been conducted to resolve general drift patterns (Hinrichsen et al., 2001a). The main objective of that study was to evaluate drift directions under different meteorological conditions. The conclusions were that the general drift is eastwards, regardless of the area in which the eggs were spawned. However, there are considerable interannual differences in drift destination, depending on windspeed, direction, and timing in relation to spawning. In years with strong westerly winds early in the year, eggs and larvae may drift within 25 d from the Kiel Bay/Danish belts as far as the Arkona and Bornholm basins. As many as 70% of all eggs and larvae could be advected into the Arkona Basin and 30% as far as the Bornholm Basin. In years with low or moderate wind during spawning, larvae seem to be retained in the spawning area. Also, situations with variable wind directions tend to retain the larvae in the spawning area. The major shortcoming of the application is that seeding of the model with drifters (i.e. eggs and larvae) and drifter behaviour (i.e. vertical migration) is not adapted to interannual variability in spatial stock dynamics, mainly through the lack of appropriate data. These variables include precise spawning areas and times, area-specific reproductive output as a result of stock composition (length distribution, sex ratio, and fecundity), precise vertical distribution of eggs, early life-stage duration, and vertical migration patterns of larvae. Predation by clupeids and ctenophores Clupeids are main predators on cod eggs in the EB (Köster and Schnack, 1994), because they occupy the same depths as most cod eggs during their daily feeding (Köster and Möllmann, 2000). For the WB, there is unfortunately no such information available. Rügen herring (Clupea harengus membras) migrate between spring-spawning areas, the Greifswalder Bodden, and feeding areas in the Sound and Kattegat/Skagerrak (Nielsen et al., 2001), and occupy depths in or below the halocline. Given this spatio-temporal overlap in distribution with spawning cod, herring are potentially significant predators on WB cod eggs (ICES, 2010). Only recently, an invasive ctenophore (Mnemiopsis leidyi) was found in the Baltic Sea (Javidpour et al., 2006). It is a known predator of fish eggs and larvae and has been incriminated in the collapse of several Black Sea fish stocks. Its appearance in the Baltic has, therefore, raised concerns about the recruitment of resident fish species, particularly cod, sprat (Sprattus sprattus balticus), and herring. In Kiel Bay, M. leidyi can reach considerable densities in autumn (Javidpour et al., 2006), but from March to the end of May, they virtually disappear, possibly because of salinity and temperatures below their level of tolerance (Kube et al., 2007; Javidpour et al., 2009a). If they bloom during the main spawning season of cod, it would be mainly during the larval stage (Javidpour et al., 2009a, b), so as a consequence of this mismatch in distribution and the absence of fish eggs in M. leidyi gut contents (Javidpour et al., 2009a), it seems to be unlikely that predation by M. leidyi is an issue in relation to recruitment of cod in the WB. This also prevents competition for food, primarily copepods (Javidpour et al., 2009a), with the larvae and early juvenile stages of cod. Human influence Only recently has the influence of human activities other than fishing come into focus as a possible factor influencing fish recruitment. Von Westernhagen et al. (1988) examined deformities in WB cod embryos from the Little Belt to Kiel Bay and Mecklenburg Bay. Most abnormalities were in the youngest eggs. A clear geographic pattern in the occurrence of abnormalities appears to exist, with prevalence in Mecklenburg Bay and south and east of Langeland. The rate of deformity varied between 18 and 32% between two consecutive years. A possible explanation for these abnormality rates may be anthropogenic pollution, particularly DDT and polychlorinated biphenyls, released into the ecosystem and the damage they cause to fish DNA (Ericson et al., 1996). This type of pollution is known to lead to reproductive failure caused by, for example, deformity, impaired development, and precipitates in the yolk (Ericson et al., 1996). Human activities often entrain a considerable load of dissolved sediments downstream. Adult cod avoid these plumes caused by, for example, marine construction, but cod eggs cannot avoid them. Eggs exposed to suspended sediments lose buoyancy in proportion to sediment concentration and exposure time (0.02 psu h 21 mg 21 l 21 ) and yolk-sac larvae suffer increased mortality at sediment concentrations of 10 mg l 21 (Westerberg et al.,1996). The impact of different concentrations depends on the sediment type, cod larvae being more sensitive to lime particles than to clay. Juvenile distribution and predation Information on the spatial and temporal distribution, behaviour, and general ecology of juvenile cod is scarce. The few studies

10 1468 K. Hüssy relating to juvenile cod (after metamorphosis) focus on distribution and cannibalism. Pihl and Ulmestrand (1993) studied the migration of juvenile cod by tagging along the west coast of Sweden and showed that they stayed close to shore and only at age 2 moved deeper. The distribution of small juvenile WB cod within the Fehmarn Belt is influenced strongly by windspeed and particularly wind direction (Bauer et al., 2010). During easterly winds, catches of juvenile cod increased, whereas westerly winds increased catches on Lolland. Whether the impact observed on juveniles is drift-related or active migration towards a habitat that is temporally more preferable as a result of the prevailing wind conditions remains unclear. However, it does confirm that juvenile cod in this area remain in shallow water. Cod is the top fish predator in the Baltic Sea ecosystem. In WB cod, cannibalism does take place, but its incidence is low (Arntz, 1977; Schulz, 1988). However, as demonstrated by Sparholt (1994) for EB cod, even a comparatively small contribution to the diet may result in considerable predation mortality at high levels of predator stock. The rates of cannibalism in WB cod seem to be negligible during most of the year, but they do increase during winter (Arntz, 1977). A possible seasonal shift in distribution towards deeper water by all sizes of cod (Oeberst, 2008) may be the direct consequence of this trend of increased cannibalism during winter. In historical times, predation on cod by seals and harbour porpoises (Phocoena phocoena) was substantial (Österblom et al., 2007). However, the abundance of these marine mammals decreased dramatically to,5% of their original population size from the beginning of the 20th century to the 1970s, and predation pressure by them on cod is, therefore, limited (Österblom et al., 2007). Summary This review of existing knowledge has identified several processes that may have implications for recruitment dynamics of WB cod. These processes are summarized briefly below and graphically in Figure 5. Within the WB, spawning areas appear to be located in specific areas in deep, saline waters deeper than m, depending on area topography. Peak spawning follows an area-specific pattern, with progressively later spawning towards the east. Adult fish show individual migration behaviours, ranging from resident to undertaking very long migrations to variable destinations. It is not known whether Baltic cod exhibit natal homing for spawning, but genetic stock structure and tagging indicate some homing. Within the Baltic Sea ecosystem, therefore, considerable mixing of stocks may be anticipated as a result of both drift of early life stages and the migrations of adult fish. The mixing of stocks seems particularly pronounced in the Arkona Basin, which may be attributable to the use of that area for spawning by both stocks, the advection of early life stages from the west, and immigration/emigration. In recent years, the size of the EB cod stock has increased, and although this has not yet been explored and explained thoroughly, there are indications that it has led to increased migration of mainly juveniles towards the west. At present, the EB and WB stocks are managed separately, and assessments do not consider spatio-temporal mixing of the two stocks. In the EB, salinity and oxygen are the key drivers of recruitment success by affecting the water depth at which cod eggs are buoyant. It is also the prevailing environmental salinity that limits the east west exchange of eggs through the differential salinity requirement of the two stocks to maintain eggs at oxygen-rich depths. Eggs of WB cod have just limited survival success in the Bornholm Basin, whereas EB eggs float too deep in the Bornholm Basin to be entrained westwards by the surface current. The drift of early life stages is therefore one of the key drivers of recruitment and stock structure in the Baltic Sea ecosystem. The drift is almost exclusively eastwards, but its magnitude and impact on the structure of the affected stocks is unresolved. Hydrodynamic modelling provides a tool to evaluate these dynamics. In contrast to the EB, hydrographic conditions in the WB do not appear negatively to influence spawning success. Conditions on the main spawning grounds are always outside the restricting thresholds, so successful fertilization and egg development are ensured. However, peak spawning seems to be influenced by temperature, with later spawning in cooler years, and may fluctuate by up to 2 months. Human activities may also influence cod recruitment by decreasing egg buoyancy and survival. In contrast to the EB, where environmental conditions are the key to reproductive success, the abundance of recruits to the WB cod stock is also influenced Figure 5. Flowchart of processes and variables influencing western Baltic cod recruitment dynamics. Dark grey, cod stocks; light grey, processes; white, parameters.