The community structure of over-wintering larval and small juvenile fish in a large estuary

Estuarine, Coastal and Shelf Science 139 (2014) 27e39

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The community structure of over-wintering larval and small juvenile fish in a large estuary Peter Munk a, *, Massimiliano Cardinale b, Michele Casini b, Ann-Christin Rudolphi b a b

Technical University of Denmark, National Institute of Aquatic Resources, Charlottenlund Castle, DK 2920 Charlottenlund, Denmark Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of Marine Research, SE 45330 Lysekil, Sweden

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 May 2013 Accepted 24 December 2013 Available online 4 January 2014

The Skagerrak and Kattegat are estuarine straits of high hydrographical and ecological diversity, situated between the saline waters of the North Sea and the brackish waters of the Baltic Sea. These sustain important nursery grounds of many fish species, of which several overwinter during the larval and early juvenile stages. In order to give more insight into the communities of the overwintering ichthyoplankton in estuarine areas, we examine an annual series of observations from a standard survey carried out 1992 e2010. Species differences and annual variability in distributions and abundances are described, and linkages between ichthyoplankton abundances and corresponding hydrographical information are analysed by GAM methods. Communities were dominated by herring, gobies, butterfish, sprat, pipefishes, lemon sole and European eel (i.e. glass eel), and all the sampled species showed large annual fluctuations in abundances. The species showed quite specific patterns of distribution although species assemblages with common distributional characteristics were identified. Within these assemblages, the ichthyoplankton abundances showed linkage to environmental characteristics described by bottomdepth and surface temperature and salinity. Hence the study points to a significant structuring of overwintering ichthyoplankton communities in large estuaries, based on the species habitat choice and its response to physical gradients. Ó 2014 Elsevier Ltd. All rights reserved.

Keywords: over-wintering ichthyoplankton fish larvae communities estuarine gradient distributional patterns

1. Introduction As transition areas between freshwater and marine systems, the estuarine areas include important nurseries of a wide range of fish species. However, the relationship between the reproductive behaviour and environmental conditions differs between species on both geographical and seasonal scales. Focused attempts to understand the background and extent of estuarine nursery grounds for marine species dates from the 1950s, where abundances of organisms were described within ranges of salinity (e.g. Günther, 1956), while more recent studies investigate the biogeographical dynamics of these areas in a specific analytical framework (Elliott and McLusky, 2002; Able, 2005). The studies might include concepts which are also used for terrestrial ecosystems, for example by describing ‘ecoclines’ which represents a gradual progressive change in the community in response to the environmental gradient (Attrill and Rundle, 2002, and references herein). The estuaries are often thought of as relative small areas

* Corresponding author. E-mail address: [email protected] (P. Munk). 0272-7714/$ e see front matter Ó 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2013.12.024

where freshwater from rivers enters the sea, (‘river mouths’, sensu Odum, 1959), however, they might also include the more offshore components, where waters are still of relatively low salinity (i.e. salinity <33.5). Such a definition takes the estuaries onto the continental shelf and widens their spatial scale significantly to an ‘estuarine zone’ which both includes the immediate estuary and the transitional areas that are consistently influenced by the water from the estuary (Elliott and McLusky, 2002; Able, 2005). The nurseries, in the sense of foraging areas of the late larval and early juvenile stages of given fish species, often extend off the immediate estuary, and studies of the bio-physical relationships must include the entire estuarine zone. The Skagerrak and Kattegat straits, situated between the Baltic Sea and the North Sea, can be interpreted as a large estuarine zone (Fig. 1). The Baltic Sea receives freshwater from a large number of rivers and this outflow inevitably has to pass through the straits. The western part of the Kattegat is a shallow plateau of approx. 10 m depth, while the eastern part is of increasing depths from 20 m in the south to about 90 m in the north. Due to the differences in depths, the western part has generally a well-mixed water column, temporarily flooded by bottom water, while the eastern part is characterised by a two-layer saltwater wedge: a net inflowing,

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P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

species that overwinter as ichthyoplankton. Feeding and growth opportunities would in this area differ significantly between the species that finish their planktonic stage during the more productive spring-summer period and the early stages of autumn spawned species which would experience a different hydrography and another plankton environment (Kiørboe and Nielsen, 1994). In order to gain further insight into habitat choice and community structuring of overwintering ichthyoplankton across estuarine zones, we here analyse the distributions of ichthyoplankton from the KattegateSkagerrak area sampled in the late winter during 20 years of observations. We investigate the speciesspecificity of distributions and for recognized communities we determine the influence of the horizontal stratification in salinity and temperature. Further, we use the series of observations to ascertain annual variability and long-term trends in the ichthyoplankton abundances. 2. Material and methods 2.1. Hydrography

Fig. 1. The study areas Skagerrak and Kattegat. The locations of three specific stations used for illustrations of hydrographic conditions are indicated.

high salinity bottom water layer and a less saline upper layer of Baltic outflow, with a significant south-north salinity gradient (Pedersen, 1993; Bendtsen et al., 2009). The water of primarily Baltic origin flows westward along the Norwegian coast in the northern part of the neighbouring Skagerrak, while more saline water of central North Sea and Atlantic origin flows eastward along the Trench slope off the Danish coast (Danielsen et al., 1997). Within this estuarine zone a wide range of fish species are found as shown by the trawl catches during the standard International Bottom Trawl Survey carried out in the area in the 1st quarter of each year (IBTS-1Q). An analysis of the catch of larger juvenile and adult species revealed high species diversity and marked differences between species in their respective distributions (Casini et al., 2005). The survey programme provides information on larger demersal fish from the standard day-time trawling but it also gives information on larvae and recently settled juveniles through a parallel night sampling by a fine meshed ring net. This sampling series of larvae and juveniles, assembled since 1992, provides a unique possibility for comparing habitat preferences of fish larvae and nursery areas of the settling juveniles across a transition area of great physical variability, and for investigating trends in the interannual variation in abundances and distributions. The IBTS-1Q survey is carried out in JanuaryeFebruary, thus much of the sampled larvae and juveniles are the overwintering stages of autumn spawning species. The larvae of autumn spawned herring are among the most numerous ichthyoplankton during the winter, and these are the main target of the ring net sampling (Anon, 2012a), but the early stages of a number of other fish species are also abundant during the winter period. Many of these are of little or no commercial importance; however they are of high ecological relevance as several are important prey for larger fish. In addition to the well-studied herring (Munk and Christensen, 1990; Anon, 2012b), little is generally known about the nursery areas of

The hydrographic measurements were carried out using a Seabird SBE 11 CTD lowered from the surface to 2 m above the bottom. Approximately 48 stations were surveyed each year. Some of the stations are included in the Swedish ‘National Monitoring Programme in the Kattegat and Skagerrak’ (see Axe et al., 2004) and three of these were used to illustrate the seasonal and annual variability in vertical stratification in February during the period 1992e2010. These stations are ‘ A16a’ (58.10
N, 10.74
E), ‘Fladen’ (57.19
N, 11.67
E) and ‘Anholt E’ (56.67
N, 12.12
E) (Fig. 1). The standard hydrographical stations were revisited several times every year during other cruises, and further hydrographic information for these is available in the ICES database (see www.ocean. ices.dk). For illustration of seasonal hydrographic variability we assembled all available information on temperature and salinity from the database at the ‘Anholt E’ station during the period 1992e 2010 from the 30 m depth stratum corresponding to the depth just below the pycnocline. 2.2. Ichthyoplankton sampling and abundance estimation Fish larvae and juveniles were sampled in the KattegateSkagerrak area during the International Bottom Trawls Survey (Anon, 2012a) on board the Swedish research vessel Argos (Fig. 1). Although this survey dates back to the early 1970s, the present investigation considers only the period from 1992 to 2010 when the same standard gear was used for sampling. The survey period was usually 3 weeks from late January to mid- February. During the survey, CTD casts were carried out during daytime while fish larvae and juveniles were sampled during night-time (only periods in complete darkness). Sampling locations of the hauls varied between years, but each year 2e5 locations were used to cover each ICES standard rectangle (1
longitude  0.5
latitude). In average 53 locations were visited each year. At each of these, oblique hauls were carried out using the ring net. The ring is of 2 m diameter, equipped with a 13 m long, black netting of 1.6 mm mesh size and uses 2 legged bridles to both the hauling wire and the depressor. A flowmeter was mounted in the opening of the net to measure the volume of water entering the net. Ships speed was set to 3 knots and the wire was paid out at a speed of 25 m min1 and retrieved at 15 m min1. The gear was towed to a minimum of 5 m above sea bottom or to a maximal depth of 100 m. The depth of the gear was measured by a gear-mounted depth sounder, while depth to bottom was estimated by a comparison to bottom depth information from the ship-mounted echo sounder. The net has a fine-meshed

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

(0.5 mm in mesh size) hind part and the same mesh in the cod-end bucket. After a haul, the hind part and cod-end were flushed and the sampled plankton and fish were collected. Fish larvae/juveniles were identified to the highest taxonomic separation and their standard lengths (clupeid and gadoid species) or total lengths (other species) were measured to the nearest mm before preservation in 4% buffered formaldehyde. The abundance of each species for each station was calculated as number of individuals per m2 as:

No m2 ¼ ðcatch=ðflow*opening areaÞÞ*depth of tow where flow and depth of tow are in m, opening area in m2. Mean abundances of each fish species for 0.5
longitude  0.25
latitude rectangles were calculated averaging station estimates within these rectangles. Overall abundances for the Kattegat and Skagerrak, respectively, were estimated by multiplying the area (in m2) by the average density estimate for all rectangles within the area. For illustration of annual variability in position of distribution centres, we calculated the centres on the latitudinal axis (LaC) as:

LaC ¼

X

ðLai  Ni Þ=Ni ;

for rectangles i (1.n), where La is latitudinal midpoint of rectangle and N is the average abundance.

2.3. Statistical analyses Linear regressions to investigate annual trends in hydrographic data were carried out using General Linear Models (GLM) in SASÒ. The association between species distributions, as estimated for the entire period, was evaluated by cluster analysis. This analysis searches for hierarchical clusters in larval/juvenile abundance in rectangles, i.e. it estimates to which extent species overlap in their “use” of given areas. We used the procedure CLUSTER in SASÒ with the Ward method of minimum variances, and the hierarchy is shown by the semi-partial squared multiple correlation; i.e. the decrease in proportion of variance accounted for due to joining two clusters. A generalized additive model (GAM, Hastie and Tibshirani, 1990) was used to statistically evaluate the effect of surface temperature, salinity and bottom depth on ichthyplankton abundance after standardising for the temporal (year) and spatial (latitude and longitude) effects. For each cluster (i.e. ‘Kattegat’, ‘Widespread’, ‘Transition area’ and ‘Skagerrak’) larvae identified to species level were used in the GAM analysis. Abundances were standardised between 0 and 1 to allow comparisons between clusters of species. Inspection of the distribution of abundances revealed a large number of low values, including true zeroes, but also occasional large catches. Thus, we used a Tweedie distribution (Tweedie, 1984) with a power-link function (p) to constrain the estimates to be positive. We used p ¼ 1.1, which is a compound Gamma-Poisson distribution which is considered appropriate for zero-inflated data (Shono, 2008). Different smoothing functions have been used for the explanatory variables. An isotropic smooth, the thin plate regression spline was adopted for modelling the effect of the interaction between latitude and longitude because of its appropriateness for modelling variables measured on the same scale as geographic coordinates (Wood, 2006). The other predictors were modelled using the thin plate smoothing spline function (Wood, 2004). All the predictors and the interaction between latitude and longitude were included in the models and a backward stepwise regression based on statistical significance and generalized cross validation (GCV; Wood, 2001, 2004) was applied to find the best set

29

of predictors and to select the final models. The least significant variable was excluded at each step of the backward stepwise regression. The GCV criterion allowed an optimal trade-off between the amount of deviance explained by the model and the model complexity measured through the equivalent degrees of freedom. Thus, the selection of the smoothing parameters for each term was done using the measure of the global GCV for the model, to balance fitting and smoothing of the data. The maximum number of knots was limited for the smoother temperature, salinity and depth (k ¼ 4) and for the interaction between latitude and longitude (k ¼ 20) to simplify the interpretation of the results. The analyses were performed using the R library mgcv (Wood, 2001; www.rproject.org). 3. Results 3.1. Hydrography The hydrography of the study area is strongly influenced by the inflow and outflow of saline and freshwater water from the neighbouring areas, the North Sea and the Baltic Sea. The general pattern is a surface outflow of relatively freshwater (salinity 20e30) through the Kattegat and a deeper inflow of saline water through the Skagerrak, but overall hydrography is complex and varies both seasonally and annually. Two years of contrasting patterns during the investigation period can be used to illustrate this hydrographical variability (Fig. 2). In 2009 the surface outflow from the Baltic was strong, and a sharp gradient in surface salinity was found in the northernmost Kattegat at the border to the Skagerrak (Fig. 2a). In 1999, on the other hand, the outflow was halted and the surface frontal zone was found further south in the Kattegat (Fig. 2c). During both years the frontal zone extended along the Swedish coast, however, the salinity gradient located offshore from the coast was much stronger in 2009 than in 1999. Generally, the outflow in the surface is counterbalanced by an inflow at larger depth of more saline water masses. Hence, in 2009 the strong surface outflow led to strong bottom inflow, and relatively high salinities were measured in the deeper water masses (Fig. 2b), while in 1999 the inflow was weaker which led to relatively lower salinity in deeper waters (Fig. 2d). During both years the strongest gradient in bottom salinity was in the Kattegat-Skagerrak border and in this area also a strong influence of the freshwater outflow from Gullmarsfjorden and adjacent fjords was apparent. The annual variability in the stratification of the water column is illustrated for the entire period 1992e2010 for three selected stations (Fig. 3). One station ( A16a) is located in the eastern Skagerrak at waters of approximately 200 m water depth, while the two other stations are located northerly (Fladen) and southerly (Anholt E) at the deeper areas (>50 m depth) of Kattegat (Fig. 1). The vertical profiles of temperature (Fig. 3a,c,e) and salinity (Fig. 3b,d,f) illustrate the marked annual variability in the depth and distinctness of the pycnocline between the fresher surface outflow and the saltier, deeper inflow. Data show general shifts in hydrographical characteristics during the period of investigation. Periods of relatively low salinity were apparent for 1993e95 and 2007e08 while the salinity was relatively high in 1996e98 and 2009e10 (Fig. 3d and f). In order to explore the annual and inter-annual hydrographic variability in more details we assembled available seasonal information for the station ‘Anholt E’. The variability is illustrated by measurements at 30 m depth, i.e. just below the pycnocline (Fig. 4). From these data it is apparent that the February observations are made during the coldest period of the year (w5
C). The seasonal variation in temperature during the years has a range of 10
C in this layer (Fig. 4a). The annual mean temperature has significantly increased about 2
C during the last two decades (GLM, seasonal

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P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

Fig. 2. Horizontal contouring of salinity at different depths in 2009 and 1999. a) 10 m depth in 2009, b) 40 m depth in 2009, c) 10 m depth in 1999, and d) 40 m depth in 1999.

effect nested in year effect, n ¼ 536, r2 ¼ 0.83, p < 0.001). The variability in salinity was more erratic, presumably related to variable strengths of inflow and outflow and, hence, to specific meteorological events (Fig. 4b). The larger perturbations in salinity, seen as a marked decline shortly after followed by an increase to above-average, were all found during mid-winter periods, and were of pronounced magnitude during the last four years of investigation. The annual mean salinity declined during the period (GLM, seasonal effect nested in year effect, n ¼ 536, r2 ¼ 0.19, p < 0.04). 3.2. Ichthyoplankton abundance and distribution We identified 40 species of fish larvae/juveniles in the samples, and in addition some specimens that only could be identified to the genus or family level. For several species catches were very sporadic, either because of low abundances or because of low catchability to the used net. These catches do not represent distribution well, and will not be dealt with here. We present period-averaged densities and total abundance estimates for 30 taxa and distributional and yearly variation for 16 of the more common taxa. Period averaged values are given in Table 1. The overall mean lengths of the different ichthyoplankton species ranged from 9 to 74 mm, and hence, catches included both relatively young larval stages and juvenile stages of the recruits of the year (Table 1). The annual variability in mean lengths of taxa is given by the standard deviation (Table 1), and we investigated potential changes during the period by linear regression. The analysis showed no significant change for all but two taxa (GLM, p > 0.10 for all these). The two taxa with significant changes in mean lengths during the period were crystal goby which showed a decline in mean length from approx. 26 to 23 mm (n ¼ 18, r2 ¼ 0.50, p < 0.001), and gobies (Pomatoschistus spp.) for which mean length increased from approx. 38e42 mm (n ¼ 18, r2 ¼ 0.49, p < 0.001).

A few species dominated, for example the primary targets of the survey, the herring larvae, were far the most abundant. The only species with abundances of the same magnitude as herring larvae were two pelagic gobies, the crystal goby (Crystallogobius minutus) and the transparent goby (Aphia minuta). Also butterfish (Pholis gunnellus), other species of gobies (Pomatoschistus spp.), sprat (Sprattus sprattus) and the pipefishes (Syngnathus spp.) were commonly caught (Table 1). Estimates of abundance of the different species showed pronounced yearly variation, apparent from patterns for the 16 taxa (Fig. 5) and low r-square values of regressions of abundance versus year (Table 1). Only a few species showed a significant change in abundance during the period (Table 1); in all these cases the abundances declined. The herring was one of these species, from 1996 the abundance of larvae in Skagerrak declined markedly from relatively high values during the early part of the investigation period (Fig. 5a). Furthermore, the abundances of glass-eel in the Kattegat/Skagerrak showed prominent changes during the period of investigation (Fig. 5e). From relatively high catches of glass-eel during 1993e95 and again in 2000, there was a marked decline and during recent years very few glass-eel have been caught. The catches of Pomatoschistus spp. also show a decline during the period, and have since 1998 been reduced by an order of magnitude (Fig. 5c). While there is no overall tendency of a decline or increase in abundance estimates of crystal and transparent goby during the period, the abundances of these two species generally follow each other, and there is a significant correlation between their abundance estimates (n ¼ 18, r2 ¼ 0.32, p < 0.05). The distributions of larvae/juveniles differed significantly between species. This appears from distributions in sub-areas averaged for the entire period (Fig. 6). The annual variability in distributions of the 16 most common species is apparent from the variability in the latitudinal distribution of midpoints (Fig. 7). Average midpoint positions of these species showed a progressive change along latitude with some inter-annual variation. The variation was evident from the 90% confidence levels which could range 0.25
latitude (Fig. 7). The similarities and dis-similarities between the period-averaged distributions are further illustrated by a Cluster analysis of relative abundances in rectangles (Fig. 8). In this analysis two groups which were either predominantly in the Kattegat or in Skagerrak differentiate clearly, and in the former a strict southerly group can be distinguished. Another group primarily covers the transition area between the Kattegat and Skagerrak (around the Kattegat Front), while other taxa were more widespread, some-in offshore areas-and some in coastal areas. We investigated the habitat characteristics given by bottom depth, temperature and salinity and of these assemblages: the taxa predominantly in Skagerrak, in Kattegat, in the transition area, and finally for the taxa that are more widespread. The used Generalized Additive Models showed an overall significant effect of depth and temperature on abundances for all investigated assemblages (Table 2). Depth had a negative effect below 20 m in ‘Kattegat’, while the effect became negative below approx. 40 m in the other areas (Fig. 9a). The positive effect levelled off at 80, 100 and 110 m depth for the ‘Kattegat’, ‘Widespread’ and ‘Transition’ areas, respectively, while the positive effect continued to the largest depths in the ‘Skagerrak’ area (Fig. 9a). The effect of temperature was generally positive (Fig. 9b). For the ‘Kattegat’ assemblage the positive response levelled off above 4
C, however, the wide 95% confidence limits for the curve above 5
C shows that this pattern was not significant at the p < 0.05 level. The effect of salinity on the abundances was significant and dome-shaped for three assemblages (Fig. 9c), when for the ‘Transition area’ assemblage there was no significant effect of salinity (Table 2). The domes were displaced among assemblages; salinity had the most positive effect at 17, 22 and 25, for ‘Widespread’, ‘Kattegat’, and ‘Skagerrak’, respectively.

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

31

Fig. 3. Vertical profiles of temperature (
C, left column) and salinity (right column) at three stations in the Skagerrak/Kattegat during the period 1991 to 2010. a) and b) Station “ A16a” (58.10
N, 10.74 E). c) and d) Station “Fladen” (57.19
N, 11.67
E). e) and f) Station “Anholt E” (56.67
N, 12.12
E). Values are indicated at depth of measurement. Stars below graphs e) and f) illustrate years of relatively deeper pycnocline.

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P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

b)

18

36 35

14

34

12

33

Salinity

16

10 8

32 31

6

30

4

29

2

28 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

Temperature

a)

Year

Year

Fig. 4. Monthly temperature (
C) and salinity measurements at 30 m depth at station “Anholt E” 1992e2011.

There was a negative effect of low salinity (<15) for ‘Widespread’ and ‘Skagerrak’, while this was not the case for the ‘Kattegat’ assemblage. 4. Discussion The present observations of the spatial and temporal hydrographic variability in the SkagerrakeKattegat supplement earlier findings (Pedersen, 1993; Jakobsen, 1997; Danielsen et al., 1997) and contribute to the general understanding of the hydrography of the area. The analysis included several stations which are part of

the Swedish National Monitoring programme, hence further description and analysis of these data is available in other publications using data from this programme (see, Axe et al., 2004). The area is obviously strongly influenced by intrusion of water masses from the neighbouring areas. Due to inflowing high salinity bottom water and the outflowing less saline upper water mass, sharp haloclines are established in both the Kattegat (eastern part) and Skagerrak (northern part), while the interaction with bottom topography lead to frontal formation especially along the southern part of the Skagerrak and between the two areas. Outstandingly high primary production has been observed both in the zone of the

Table 1 Information on the most common ichthyplankton species caught during IBTS-1Q between 1992 and 2010. Species ranked according to averaged yearly abundance. Mean abundance in Kattegat (no per 103 m2)

Mean abundance in Skagerrak (no per 103 m2)

Overall abundance (no* 106)

1.6 2.6 2.8 2.2 8.8

27.931 62.602 66.409 52.358 22.972

228.647 195.761 31.932 5.489 3.555

7931 7642 2483 1328 619

8 18 59 87 82

0.02 0.41 0.03 0.06 0.50

0.61 0.003* 0.46 0.33 0.001*

19.7 10.7 1.9 2.8 0.7 9.7 1.9 12.2 4.4 9.3 1.3 12.1

8.385 2.661 5.590 7.220 1.176 6.215 0.069 1.998 0.052 3.761 0.034 0.649 0.610

5.023 8.979 4.578 1.496 4.291 0.527 3.968 1.927 2.922 0.011 0.569 0.063 0.052

345 346 269 207 163 154 129 106 95 83 19 16 15

53 17 46 77 16 89 1 42 1 100 4 88 89

0.13 0.08 0.01 0.01 0.11 0.02 0.24 0.38 0.10 0.01 0.13 0.07 0.18

0.13 0.24 0.72 0.74 0.17 0.53 0.032* 0.005* 0.20 0.81 0.14 0.28 0.07

62.8 51.1 17.8 57.7

15.4 9.5 6.9 7.9

0.067 0.165 0.317 0.157

0.391 0.315 0.021 0.123

14 14 8 7

11 26 91 47

0.07 0.09 0.13 0.01

0.28 0.22 0.13 0.88

47.1 51.8 24.3 21.0 13.7 e 68.5 27.0

8.3 9.4 1.9 e 1.8 e e 5.6

0.186 0.225 0.057 0.000 0.069 0.020 0.009 0.053

0.103 0.051 0.061 0.065 0.000 0.029 0.033 0.000

7 7 3 2 2 1 1 1

55 75 39 0 100 32 15 100

0.11 0.12 0.06 0.04 0.08 0.10 0.07 0.01

0.16 0.15 0.32 0.43 0.25 0.20 0.28 0.87

Taxon

English name

Overall mean length (mm)

Crystallogobius linearis Clupea harengus Aphia minuta Pholis gunnellus Pomatoschistus spp.

Crystal goby Atlantic herring Transparent goby Butterfish Gobies (Common, Painted or Sand) Sprat Nilssons pipefish Sandeels Yarrell’s blenny Lemon sole Short horn sculpin Pearlside European eel Silver smelts Hook-nose Snake pipefish Sea scorpion Four-bearded rockling Long rough dab Dragonets Hakes Three-spined stickleback Witch Solenette Atlantic wolf-fish Mullets Snake blenny Gurnards Worm pipefish Scaldfish

23.9 29.1 34.3 14.9 40.6 43.6 67.4 43.2 17.1 26.8 8.7 33.5 74.2 36.3 10.0 60.4 8.2 23.2

Sprattus sprattus Syngnathus rostellatus Ammodytidae Chirolophis ascanii Microstomus kitt Myoxocephalus scorpius Maurolicus muelleri Anguilla anguilla Argentina spp. Agonus cataphractus Entelurus aequoreus Taurulus bubalis Enchelyopus cimbrius Hippoglossoides platessoides Callionymus spp. Phycidae Gasterosteus aculeatus Glyptocephalus cynoglossus Buglossidium luteum Anarhichas lupus Mugilidae Lumpenus lampretaeformis Triglidae Nerophis lumbriciformis Arnoglossus laterna

STD of yearly mean lengths (mm)

Prop. of pop. in Kattegat (%)

Statistics on annual trend in abundance (n ¼ 19 for all)) r-square Pr > F

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

a)

40

b)

33

25

Clupea harengus Sprattus sprattus

Crystallogobius linearis Aphia minuta 20

Abundance (x 10 )

30

15 20 10

10 5

0

0 1995

c)

2000

2005

2010

1995

d)

4

Pholis gunnellus Pomatochistus spp.

1.4

Abundance (x 10 )

3

2000

2005

2010

2005

2010

1.6

Syngnatus spp. Microstomus kitt

1.2 1.0

2

0.8 0.6

1

0.4 0.2

0

e)

0.0 1995

2000

2005

2010

f)

1.0

1995

2000

0.8

Ammodytes spp. Agonus cataphractus

Chirlophis ascanii Anguilla angullia 0.8

Abundance (x 10 )

0.6

0.6 0.4 0.4

0.2 0.2

0.0

0.0 1995

g)

2000

2005

2010

1995

h)

0.8

Enchelyopus cimbrius Myoxocephalus scorpius

2000

2005

2010

2005

2010

0.20 0.18

Taurulus bubalis Callionymus spp.

0.16 Abundance (x 10 )

0.6 0.14 0.12 0.4

0.10 0.08 0.06

0.2 0.04 0.02 0.0

0.00 1995

2000 Year

2005

2010

1995

2000 Year

Fig. 5. Yearly variation in abundance (no  106) of 16 common ichthyoplankton taxa during the period 1992e2010.

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P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

Fig. 6. Horizontal distribution of 16 common ichthyoplankton taxa during IBTS in February between 1992 and 2010. Abundance estimates averaged in rectangles of 0.25
latitude and 0.5
longitude for all years 1992e2010. Areas of circles illustrate relative abundance for each taxa.

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

Fig. 6. (continued).

35

36

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39 59.0

Latitude N

58.0

57.0

Microstomus kitt

Crystallogobius linearis

Clupea harengus

Anguilla anguilla

Syngnathus spp.

Callionymus spp.

Aphia minuta

Ammodytes sp.

Sprattus sprattus

Pomatoschistus sp

Taurulus bubalis

Chirolophis ascanii

Pholis gunnellus

Myoxocephalus scorpius

Agonus cataphractus

Enchelyopus cimbrius

56.0

Fig. 7. Box plot of variability in position of latitudinal midpoints for 16 common ichtyoplankton taxa. Mean shown by heavy horizontal line, median by thin line, the box enclose the 75%, and the whiskers the 95% confidence interval.

northern Kattegat front and in the slope front in the Skagerrak (Richardson, 1985; Munk et al., 1995). The present clustering and GAM analyses suggested a marked structuring of the ichthyoplankton community, related to geography and bottom depth, but also strongly influenced by the hydrographical conditions as measured during the time of sampling. We could identify assemblages with common characteristics, however we also found a gradual progressive change in the community in response to the environmental gradient given by surface salinity. Some species were predominantly found in the low-saline southernmost part of the investigation area, while other were restricted

to the more saline areas in the north, and between these we found a wide range of other distributional patterns. Such structuring of fish assemblages across a salinity transition has been observed in a number of other estuarine zones (e.g. Jung and Houde, 2003; Martino and Able, 2003). The differences between the distinguished assemblages in their response to salinity are apparent from the GAM analysis. Except for the assemblage in the dynamic transition area of the Kattegat front, salinity had a positive effect on abundances across a wide range of intermediate surface salinities, while outstanding low or high salinities had a negative effect on abundance. This pattern indicates that, within its common habitat, the ichthyoplankton tolerates a certain degree of salinity variation, while it would be largely affected in extreme situations of salinity change. Temperature has generally a strong positive effect on abundances across the entire temperature range, which indicates that warmer winters and stable salinity are advantageous to the overwintering of ichthyoplankton. While our observations of hydrographic variability during the past 20 years showed generally warmer winters, more extreme low-salinity events and a generally declining salinity were indicated for recent years. Hence, there might both be positive and negative impacts of the hydrographic changes in the area, changes that probably are linked to the trend of climate change (OSPAR, 2010). There are only few comparable studies on ichthyoplankton from the Kattegat/Skagerrak area. Christensen et al. (1984) studied distribution patterns of fish larvae in the area during April 1983. During this time of the year the young larvae of the springspawning species are abundant, and hence, most of the species covered by that study were not sampled during our study. Cod (Gadus morhua), sandeel (Ammodytes marina), dab (Limanda limanda) and plaice (Pleuronectes platessa) were the most abundant larval species in April. Of these species the dab and plaice larvae were concentrated in the Northern Kattegat front, while cod were abundant in the deeper areas of Kattegat. Sandeel were more widespread along the coasts of Sweden and Norway, however, with peaking abundance in the area of the Northern Kattegat Front.

Agonus cataphractus Myoxocephalus scorpius Pholis gunnellus Chirolophis ascanii Pomatoschistus sp Enchelyopus cimbrius Taurulus bubalis Ammodytidae Phycidae Aphia minuta Lumpenus lampretaeformis Glyptocephalus cynoglossus Hippoglossoides platessoides Buglossidium luteum Gasterosteus aculeatus Callionymus spp Gobiidae Anguilla anguilla Sprattus sprattus Clupea harengus Microstomus kitt Syngnathus spp Mugilidae Argentina spp Crystallogobius linearis Maurolicus muelleri Entelurus aequoreus 0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

Semi-Partial R-Squared Fig. 8. Dendrogram of cluster analysis results. Hierarchy is shown by the semi-partial squared multiple correlation, identified major assemblages are indicated.

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

37

Table 2 GAM results using tweedie distribution with power-link and ichthyoplankton abundace as response. Results on four assemblages named by areas of primary distribution. df

Variable

Kattegat 8.9 Year 18.0 Latitude:longitude 2.8 Temperature 2.8 Salinity 2.5 Depth Transition area 8.8 Year 17.7 Latitude:longitude 2.1 Temperature 1.0 Salinity 2.9 Depth

F

P

n ¼ 5658; DEV ¼ 29.1% 36.9 <0.0001 9.2 <0.0001 53.9 <0.0001 35.8 <0.0001 10.2 <0.0001 n ¼ 3772; DEV ¼ 33.7% 72.2 <0.0001 17.1 <0.0001 29.1 <0.0001 0.7 ns 37.7 <0.0001

Hence, Christensen et al. (1984) showed the same species specificity of distributional patterns during April as shown in our study, and they also pointed to the importance of the Northern Kattegat Front. The effect of frontal processes on distributional patterns of ichthyoplankton in the Skagerrak and Kattegat is further highlighted in a study of gadoid species from May 1991e94 (Munk et al., 1999). During this study, the distributions of larvae and small juveniles consistently followed the frontal hydrography while the abundance of each species peaked in different parts of the frontal zone. High abundances of all species were found along the southern Skagerrak, in the Northern Kattegat Front and along the Swedish coast. This pattern of distribution, with a close linkage to the frontal zone along the periphery of Skagerrak, agrees with the present observations for e.g. herring, sprat and lemon sole. We found fish larvae/juveniles of a wide range of sizes, and accordingly the species were of variable stage of development. The observed differences in mean lengths between species were generally in agreement with reported main spawning times for the respective species (Munk and Nielsen 2005). This can be illustrated by the findings for three size groups, larvae of 8e20 mm, larger larvae of 20e30 mm and the early juveniles of >35 mm. The 8e 20 mm group, which include species as snake blenny (Lumpenus lampretaeformis), hook-nose (Agonus cataphractus), short horn sculpin (Myoxocephalus scorpius), Yarrells blenny (Chirolophis ascanii) and butterfish have reported peak spawning times from January to March. Hence, we probably caught the early hatched specimen of these winter spawned species. The 20e35 mm group, including species as crystal goby, transparent goby, herring, lemon sole and pearlside (Maurolicus muelleri) are from the summer spawning, primarily July to October, and hence in an age range of about 4e7 months. Finally, the larger sized species (>35 mm) as sprat, long rough dab, silver smelt (Argentina spp.) and witch are predominantly spring-spawned (April to June). This latter group was probably not caught representatively, since it is likely that we only caught the smallest specimens of the full size range of the species. Similarly there were a number of other spring spawned species that was not caught primarily because of their large size and/or demersal behaviour, for example the common gadoid juveniles. Our estimated densities of larvae and juveniles were generally in the lower range compared to other studies. The maximal densities were in the order of 0.2 m2, which is somewhat lower than the mean densities observed during other investigations in the area. For example mean densities of larger gadoid larvae in the Skagerrak during May was estimated to 0.3e0.7 m2 (Munk et al., 1999), and the densities of newly hatched larvae in April reported by Christensen et al. (1984) was several magnitudes higher. However we would expect significant reduction in abundance for the older overwintering stages due to the high mortality during the

df Widespread 8.8 17.8 1.0 2.7 2.6 Skaggerak 8.4 17.1 1.0 2.6 2.9

Variable Year Latitude:longitude Temperature Salinity Depth Year Latitude:longitude Temperature Salinity Depth

F

P

n ¼ 4415; DEV ¼ 27.4% 30.3 <0.0001 31.1 <0.0001 140.9 <0.0001 15.2 <0.0001 5.0 <0.002 n ¼ 2469; DEV ¼ 36.3% 18.4 <0.0001 5.3 <0.0001 46.7 <0.0001 15.5 <0.0001 71.4 <0.0001

early larval phase and the generally more dispersed distribution during later stages. We also observed pronounced year-to-year variability in abundance estimates of larvae. A large part of the variability observed for the less abundant species could be due to sampling variability. For the more abundant species, we will expect a reasonable coverage of larval abundances and hence that the estimates express year-to-year variability. Annual variability in abundance might reach an order of magnitude, as for example a pronounced increase for Nilsson’s pipefish (Syngnathus rostellatus). We also observed a few years with increasing abundance of another pipefish species, the snake pipefish (Entelurus aequoreus), in accordance with other observations of boosting abundances of this species during the period 2005e08 (Harris et al., 2007; van Damme and Couperus, 2008). We only found temporal trend in the abundance estimates for a few species, and these showed a general decline during the investigated period. The two commercially important species, herring and European eel, have almost disappeared in the Kattegat/ Skagerrak during recent years. The stocks of these species have their main spawning and nursery sites outside the area (Munk and Christensen, 1990; Tesch and White 2008), and the abundances in our investigation area represent only a fraction of their population. Hence, the declining abundances of these species could be due to either a general decline in recruitment of the species or a reduced influx from other areas. For both herring and eel, recruitment to the populations has declined markedly during the period (Anon, 2011, 2012b). For herring the reduction of recruitment has been to approx. 30% of the early 1990s level, although the North Sea herring population from which the larvae sampled here derive is still considered in good condition (Anon, 2012b). Hence, the very low numbers of herring larvae caught in the investigated area is partly due to the general decline, but likely also due to changes in the fraction of the population which drift into the area. The abundances of recruiting glass eels have been reduced at least one order of magnitude across the entire Europa following the collapse of the eel stock (IUCN, 2012), hence the disappearance of the glass-eel in catches from the present surveys is in correspondence to the largescale decline in overall recruitment. While we found a large annual variability in abundances of single species, and significant effect of environmental variables on assemblages, we found no tendency of a general change in habitats of given species. The general fish larval community pattern was retained during the two decades of observation, a pattern that was linked to the environmental gradient of salinity, seen as a general increase through the Kattegat and along the northern part of Skagerrak. This interplay apparently establishes a series of communities of different composition, a pattern described as an ecocline by Attrill and Rundle (2002). Hence, the structuring of ichthyoplankton communities across estuarine zones, which has primarily

38

P. Munk et al. / Estuarine, Coastal and Shelf Science 139 (2014) 27e39

Aquatic Resources) of the Swedish University of Agricultural Sciences, for long-time high-quality data collection during the Swedish part of IBTS. All hydrographical measurements were taken onboard by the Swedish Meteorological and Hydrological Institute (SMHI), Oceanographic Laboratory. Fish larvae identification was performed by Ann-Christin Rudolphi (responsible), Karin Frohlund and Anne-Marie Palmén Bratt. References

Fig. 9. The effect of three parameters on the abundances of four ichthyoplankton assemblages, results from GAM analyses. The effect is shown by negative and positive values, separated by a horizontal line. Average effect shown by line, 95% confidence interval by shaded area. Inward tick marks on x-axes illustrate available values. Effect of a) bottom depth (m), b) temperature (
C) and c) salinity.

been described for newly hatched larvae during the productive spring and summer period, is also apparent for the assemblages of species that overwinter as larvae or small juveniles. Acknowledgements We thank the personnel at the former Swedish Board of Fisheries, and at the current Institute of Marine Research (Dep. of

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