Estuarine, Coastal and Shelf Science 67 (2006) 123e132
                                                              www.elsevier.com/locate/ecss




           Shift in fish assemblage structure due to loss of seagrass
                Zostera marina habitats in Sweden
      Leif Pihl a,*, Susanne Baden a, Nils Kautsky b, Patrik Ronnback b, Tore Soderqvist c,
                                  ¨  ¨      ¨
                         c          a
                           ˚
                   Max.Troell , Hakan Wennhage
         a
          Department of Marine Ecology, Goteborg University, Kristineberg Marine Research Station, 450 34 Fiskebackskil, Sweden
                            ¨                                  ¨
                    b
                     Department of System Ecology, Stockholm University, 106 91 Stockholm, Sweden
         c
          Beijer International Institute of Ecological Economics, The Royal Swedish Academy of Science, 10405 Stockholm, Sweden
                           Received 6 June 2005; accepted 14 October 2005
                               Available online 19 January 2006




Abstract

  The areal extent of Zostera marina in the archipelago of the Swedish Skagerrak has decreased by 60% over two decades. To investigate the
effects of Z. marina loss on the local fish assemblages, the fish fauna was compared between existing seagrass beds and sites where seagrass had
vanished. A field study was carried out at four shallow locations in the outer archipelago of the coast in June 2004. Within each location two sites
were sampled, one with an existing Z. marina bed and another where Z. marina had disappeared. Fish were sampled semi-quantitatively with
a beach seine. Samples were taken during both day and night and captured fish were examined to species, enumerated and measured in the field,
and released thereafter. The number of fish species was found to be significantly higher in Z. marina habitats compared to areas where seagrass
was missing, and density and biomass of fish were generally lower in areas dominated by bare sediment compared to those in the seagrass hab-
itats. Several species and groups of fishes (i.e., gadoids, labrids, syngnathids) were absent or occurred in low densities at sites where Z. marina
was missing. For example, juvenile 0-group cod density was reduced by 96% at sites where Z. marina had disappeared. Such a reduction in
recruitment of cod is in the same order of magnitude as the combined effect of seal predation and mortality due to by-catches in the eel
fyke-net fishery estimated for the archipelago of the Swedish Skagerrak. Hence, the results clearly indicate a shift in the fish assemblage, in-
cluding a loss of taxa at the family level as a result of degradation in habitat-forming vegetation.
Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: habitat loss; eutrophication; cod; plaice; Skagerrak




1. Introduction                                 are considered to be higher compared to alternative habitats
                                        (Beck et al., 2001; Deegan et al., 2002).
  Seagrass meadows provide habitat diversity in the coastal           The global loss of seagrasses from the mid-1980s to the
seascape worldwide. This habitat-forming vegetation creates           mid-1990s has been estimated to be 12,000 km2 (Short and
a three dimensional architecture over soft bottoms, which sta-         Wyllie-Echeverria, 1996), which correspond to an overall re-
bilizes the sediment and reduces water movements. Seagrass           duction by about 7% of the total areal extent (Spalding
meadows are known to harbour a diverse and abundant fauna            et al., 2003). This fact has contributed to the listing of seagrass
of invertebrates and are generally considered as essential hab-         beds as habitats worthy of protection in the Rio-declaration
itats for many fish species (Orth et al., 1984; Jenkins et al.,         (1992/93:13). The consensus from the report ‘‘World Atlas
1997). Fish may spawn in seagrass beds or use the area as            of Seagrasses’’ is that the main reasons for the decline, apart
a nursery ground, where growth and survival of juvenile fish           from natural threats such as storms and diseases, are anthropo-
                                        genic (Green and Short, 2003). Most serious are the indirect
                                        effects of human activity. Increased turbidity and overgrowth
* Corresponding author.                            by epiphytic algae reduce light penetration, resulting in subse-
  E-mail address: leif.pihl@kmf.gu.se (L. Pihl).                quent loss of seagrass. Turbidity and surplus algal growth may

0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2005.10.016
124                 L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132

derive from physical disturbances on land or in the water, and       however, hard to evaluate and there may be alternative explan-
from eutrophication combined with trophic cascades (e.g. ef-        ations for the changes observed (Orth et al., 1996; Browder
fects of over-fishing) in the coastal ecosystem (Howarth          et al., 1999). To our knowledge there is only one study com-
et al., 2000; Jackson et al., 2001; Hughes et al., 2004). Direct      paring areas with extant and lost seagrass habitats (Hughes
disturbances such as dredging and benthic trawling in seagrass       et al., 2002). The study, performed in estuaries along the
will most likely cause drastic local effects, but are probably of     NW Atlantic Coast, reported that the abundance, biomass
less importance on a larger scale compared to more diffuse, in-      and species richness of fish were lower in areas where seagrass
direct anthropogenic affects (Hily et al., 2003).             beds had disappeared, but the generality of these findings for
  Zostera marina is the dominant seagrass species in Swedish       other coastal areas are not known.
coastal waters. Along the SkagerrakeKattegat coast, it occurs         The aim of this study was to investigate the effects of losses
in semi-exposed and protected areas within water depths of         of Zostera marina on the local fish assemblages on the Swedish
0.5e6 m (Baden and Bostrom, 2001). These Zostera beds
                ¨                     west coast. This was carried out by comparing the fish fauna in
have been shown to support a high production of benthic fauna       existing seagrass beds with sites where seagrass has vanished
as well as epibenthic invertebrates and fish (Baden and Pihl,        over the last two decades. The main purpose was to document
1984; Moller et al., 1985), and to serve as nursery and feeding
     ¨                                shifts in fish assemblages through measurements of species
grounds for more than 40 fish species (Pihl and Wennhage,          numbers, densities and biomass. By comparing the utilization
2002; Wennhage and Pihl, 2002). Over the last two decades,         by fish of Z. marina beds and alternative habitats, changes in
a 60% reduction in distribution of the Z. marina has been ob-       the ecological function of coastal areas with loss of seagrass
served in the Swedish Skagerrak archipelago (Baden et al.,         could be evaluated.
2003). Along most sections of the coast both the upper and
the lower depth distributions of seagrass have been reduced,
resulting in a narrowing of meadows, but in some areas sea-        2. Methods
grass meadows have disappeared completely. The lost Z. ma-
rina is commonly replaced by a bare sediment bottom, but            This field study was carried out in the outer archipelago of
in some areas the sediment is partly covered by filamentous         the Swedish Skagerrak coast (58  14e220 N; 11  23e320 E)
green algae or patches of Fucus spp., attached to shells and        (Fig. 1) between 8 and 20 June 2004. The archipelago consists
stones. The reason for the degradation of the seagrass habitat       of islands of varying size, and a shoreline characterized by
in the Skagerrak is not known, but coastal eutrophication and/       a mixture of rocky and soft-bottom substrata. On soft bottoms
or over-fishing have been suggested as plausible causes. In ad-       Zostera marina is the dominating vegetation within the depth
dition, altered water exchange due to construction of road         range of 1e5 m (Baden et al., 2003). This coastal region is
banks and leisure boat harbours could have reduced the distri-       micro-tidal with a tidal amplitude of around 0.2 m. Mean sur-
bution of seagrass in the coastal Skagerrak.                face water temperatures usually range from 5 to 15  C in
  Historical distribution maps of seagrass from Scandinavia       spring and autumn and from 15 to 20  C during the summer
are few, but extensive Danish investigations dating back to        (Pihl and Rosenberg, 1982). Surface water salinity typically
1900 reveal that only about 25% of the former areal extension       fluctuates between 20 and 25 psu in the summer.
remained in 1990 (Petersen, 1914). This large areal reduction         June was selected for sampling in this investigation because
is partly attributed to losses of deep eelgrass stands as a conse-     previous studies on seasonal dynamic of the fish community
quence of impoverished light conditions and partly to the slow       had shown that the highest species richness, abundance and
recovery after the seagrass disease in the 1930s. Between 1900       biomass occurred at that time of the year (Pihl and Wennhage,
and 1990, maximum colonisation depths decreased from            2002). In June most of the fish are recruited to the coastal hab-
5e6 m in estuaries and 7e8 m in open waters, to 2e3 m           itats, giving a full representation of age-classes in the fish
and 4e5 m, respectively (Bostrom et al., 2003).
                  ¨                    community. The investigated coastal region represents one
  The change in habitat structure following the loss of         of five areas where Zostera marina has been observed to de-
a Zostera marina bed is likely to shift the local system into       crease significantly in its distribution over the last two decades
an alternative state. Primarily, the loss of the habitat-forming      (Baden et al., 2003). Within this region four locations were
species Z. marina will alter habitat complexity, changing the       chosen at random and two sites were selected in each: one
structure of associated fauna assemblages. In a review of the       with an existing Z. marina bed and another where Z. marina
extensive literature testing the importance of seagrass mead-       had disappeared (Fig. 1). Sites with existing seagrass were
ows as nursery areas for juvenile fish and invertebrates,          chosen in close vicinity (about 500 m) to the sites without sea-
Heck et al. (2003) found that their abundance, growth and sur-       grass. At the seagrass sites each Z. marina bed had a spatial
vival were generally higher in seagrass compared to unstruc-        distribution of more than 10 ha, covering 60e100% of the
tured habitats, but similar to other structured habitat,          bottom area within the depth range of 1e4 m. At sites where
indicating that habitat complexity may be more important to        Z. marina had disappeared compared to the 1982 distribution,
fish diversity than the type of structures present. There are        the bottom sediment was generally free of vegetation, except
also a few studies more specifically reporting changes in spe-       from sparse occurrence of Z. marina shoots and small patches
cies composition following large-scale losses of seagrass beds.      of Fucus spp. stands. Vegetation cover at these sites was
Historical comparisons without appropriate controls are,          1e15% of the bottom area.
                    L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132                125




      Fig. 1. Map of the investigated area in the archipelago of the Swedish Skagerrak. Sampling locations indicated by open circles.


  A sampling area of 5 ha was designated in the centre of          haul during the night (24e01 hours) in each of the investigated
each selected site. Fish were sampled semi-quantitatively           sites. Sampling order was randomly allocated between sites
with a beach seine according to Tveite (1984), a method            and over time to avoid introduction of systematic errors.
most commonly used to study fish communities in the littoral          Day and night samples were taken at random in the designated
zone. The method has the advantage of allowing for estimates         area, and !50 m apart within a site. Captured fish were exam-
of the area being sampled; a feature not shared by some other         ined to species, enumerated and measured (total length, mm)
methods in use (e.g. gillnets and fyke-nets). Methodological         in the field, and released thereafter. Some fish from three large
studies have shown that benthic species and small-size individ-        samples collected at night were brought to the laboratory for
uals may hide within substrata having a high complexity or es-        further analysis. Estimates of the biomass (wet wt.) for all in-
cape underneath the foot-rope of the seine (Parsley et al.,          dividual fishes were derived from established lengtheweight
1989). Beach seines may also have selectivity towards             relationships. In addition to fish, macro-crustaceans (mainly
small-sized species, at least in comparison to other methods         shrimps and crabs) were also collected. Numbers and pooled
(Pierce et al., 1990; Weaver et al., 1993). However, the beach        biomass (wet wt.) for each species of invertebrates were re-
seine maintains its performance better than visual sensing          corded for each sample in the laboratory.
techniques when macrophyte cover increases (Brind’Amour              Shoot density, mean and maximum length and biomass of
and Boisclair, 2004). The seine was 40 m long, 3 m high,           Zostera marina were estimated in the four seagrass beds.
had a mesh opening of 10 mm in the arms and 5 mm in the            Three quantitative samples were taken by a diver using
‘‘cod end’’ and was towed by 30 m long ropes. The gear            a net-bag (mesh opening 1 mm) connected to a bottom metal
was deployed from a small boat in a rectangular shape with          ring (diameter of 35 cm). Samples were allocated randomly in
its deepest part at around 3 m depth. It was pulled shoreward         the centre of the Z. marina bed at approximately 2 m depth.
33 m by four people 15 m apart until reaching a water depth of        Percentage cover of Z. marina was visually assessed by a diver,
1 m, giving an effective fishing area of approximately 500 m2.         swimming over the investigated area. At sites where Z. marina
One haul was taken during daytime (12e13 hours) and one            had disappeared, the vegetation cover was assessed visually
126                 L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132

from the boat before sampling. To characterize the sediment        Table 1
substrate three quantitative sediment cores were collected ran-      Shoot density, blade length and biomass (wet wt.) of Zostera marina, and cov-
                                      er of Z. marina and Fucus spp., as well as sediment organic content (%) in the
domly by a diver in each of the study sites (1e3 m water          eight sample sites
depth) for analysis of organic content. Samples of the upper
                                                     Brofjorden  Lindholmen   Finnsbo   ˚ ¨
                                                                         Gaso
2 cm of the sediment core were dried at 60  C for 24 h and
combusted for 4 h at 450  C, and organic content was mea-         Zostera marina sites
                                      Cover of Zostera (%)      100      60      100    100
sured by weight loss.
  Fish assemblage structure was compared between samples         Number of shoots
                                       Mean (g dw mÿ2) (n ¼ 3)   230     100       380    250
by using BrayeCurtis similarity indices, as described in the
                                       SE              36      21       21     50
PRIMER package (Field et al., 1982). Fish abundance data
were log(X þ 1) transformed to weigh the relative numerical        Blade length
                                       Mean (cm) (n ¼ 3)       47.2     30.1      22.1    39.8
importance of common and rare species in the analysis.            SE               4.6      2.3      1     3.9
BrayeCurtis similarity indices were computed and the result-         Max (cm)           104      67       39     66
ing similarity matrix was used to perform non-metric Multi-
                                      Blade biomass
Dimensional Scaling (MDS). An analysis of similarities            Mean (g dw mÿ2) (n ¼ 3)   172.2     43.5      71.2   141.2
(ANOSIM) was used to test for differences in assemblage           SE              13.8     21.5      11.3    31.4
structure between the two habitat types, and to compare day        Sediment org. content
and night samplings (method in Clarke, 1993). The propor-          Mean (%) (n ¼ 3)       16.6     14.5      1.7    13.6
tional contribution of different fish species to the dissimilarity      SE               1.3      0.6      0.1    0.8
between groups was investigated using SIMPER (method in
Clarke and Warwick, 1994). Fish abundance, biomass and           Non-Zostera marina sites
                                      Cover of Zostera (%)       0       0       1     0
number of species in the two habitat types were compared us-
ing two-way ANOVAs, with habitat and time of day as factors.        Cover of Fucus spp. (%)     5     10e15       0    5e10
Non-transformed data used as variances were shown to be ho-        Sediment org. content
mogenous according to Cochran’s test.                    Mean (%) (n ¼ 3)        5.4      3.3      1     1.3
                                       SE               0.5      0.4      0.06    0.06

3. Results
                                                                 ˚ ¨
                                      two areas, one was considered as semi-exposed (Gaso) and
3.1. Vegetation                              one had a high physical exposure (Finnsbo). In the protected
                                      and semi-exposed areas, content of organic matter in Zostera
  In three out of four Zostera marina beds investigated the        marina beds varied between 13.6 and 16.6%, whereas the ex-
vegetation had a homogenous density with full cover of the sed-      posed Z. marina bed had a sandy sediment with only 1.7% or-
iment. Only at one site, Lindholmen (location 2), the Z. marina      ganic content (Table 1). At the sampled sites mainly free of
had a patchy distribution covering approximately 60% of the        vegetation content of organic matter in the sediment was esti-
sediment. Mean shoot density was estimated to be 100e           mated to be between 1.0 and 5.4%, with the highest value in
380 shoots mÿ2 in the four Z. marina beds, the lowest densities      the protected areas (Table 1). Thus, organic content in the sed-
occurring at the site where the bed had a patchy distribution       iment was 2e10 times higher in Z. marina beds compared to
(Table 1). The mean blade length varied from 22 to 47 cm at        unvegetated sites, but inter-location differences could be im-
the four sites, and maximum length was about double the          portant due to variation in exposure.
mean length at all sites (Table 1). Blade biomass of Z. marina
was found to be between 44 and 172 g dw mÿ2 at the study sites,
                                      3.3. Fish
with the lowest values in the beds having either low mean blade
length or a patchy distribution. At the four sites where Z. marina
                                        Altogether, 33 fish species belonging to 15 families were
beds had disappeared over the last two decades the sediment
                                      identified in this investigation (Table 2). Twenty-eight species
was mainly free of vegetation. At one site (the exposed area
                                      were found in the Zostera marina beds, of which nine were ex-
Finsbo, location 3) a few remaining shoots of Z. marina were
                                      clusive to this habitat. At the sites where Z. marina had disap-
found covering around 1% of the bottom (Table 1). The other
                                      peared 19 fish species were found, and five of these species
three sites had patches of Fucus spp. growing on stones and
                                      were only found here. When comparing Z. marina and non-
shells of blue mussels with an approximate cover of between
                                      seagrass sites in pairs for each location, the number of fish spe-
5 and 15% of the bottom sediment.
                                      cies was in all cases higher in the Zostera habitat (Fig. 2).
                                      Overall the number of fish species was significantly higher
3.2. Sediment                               ( p < 0.005) in Z. marina beds than at non-seagrass sites, but
                                      no difference was observed between day and night samplings
 Two of the investigated locations (Brofjorden and Lindhol-        (Table 3). The mean number of individuals sampleÿ1 exhibited
men) were situated in an enclosed part of the archipelago and       a large variation between locations and sites (Fig. 2). Generally,
were protected from exposure to wind and waves. Of the other        the numbers of individuals were higher in catches from
                       L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132                    127

Table 2
Number of individuals and biomasses (wet wt.) of fishes recorded in beach-seine samples. Pooled data of day and night samples from four Zostera marina sites, and
from four sites where Z. marina has disappeared
Family            Fish species               Numbers                      Biomass
                                    Zostera        Non-Zostera         Zostera         Non-Zostera
                                    marina         marina           marina          marina
Anguillidae          Anguilla anguilla             12           23              456.4         1436.7
Gobiidae           Aphia minuta               1423          169             4705.5         261.0
Callionymidae         Callionymus lyra              0           1               0.0          11.5
Clupeidae           Clupea harengus               1           84               2.6         157.4
Labridae           Ctenolabrus rupestris           272           2             2062.8          17.7
Syngnathidae         Entelurus aequoreus            16           0              70.1          0.0
Gadidae            Gadus morhua               146           12              947.1         1142.7
Gasterosteidae        Gasterosteus aculeatus          1164          916             1781.7         1527.6
Gobiidae           Gobius niger               738          304             4605.1         924.1
Gobiidae           Gobiusculus flavescens           264           0              137.3          0.0
Pleuronectidae        Limanda limanda               5           0              228.3          0.0
Gadidae            Merlangius merlangus            16           0              482.1          0.0
Cottidae           Myoxocephalus scorpius           22           2              868.9          81.6
Syngnathidae         Nerophis lumbriciformis           1           1               2.6          5.5
Syngnathidae         Nerophis ophidion             32           4              25.1          2.3
Pholidae           Pholis gunnellus              3           0              42.5          0.0
Pleuronectidae        Platichthys flesus             11           37             2206.6         1835.4
Pleuronectidae        Pleuronectes platessa           21          143              74.8         310.8
Gadidae            Pollachius virens              4           0              11.0          0.0
Gobiidae           Pomatoschistus microps           0           90               0.0          85.1
Gobiidae           Pomatoschistus minutus           30           72              75.6         178.6
Gobiidae           Pomatoschistus pictus           16           18              23.6          23.5
Salmonidae          Salmo trutta                9           4              785.4         777.8
Bothidae           Scophthalmus rhombus            0           1               0.0          0.2
Soleidae           Solea solea                 0           1               0.0          48.8
Gasterosteidae        Spinachia spinachia             2           0               8.4          0.0
Labridae           Symphodus melops              4           0              62.8          0.0
Syngnathidae         Syngnathus acus              35           0              179.2          0.0
Syngnathidae         Syngnathus rostellatus           33           23              38.0          27.3
Syngnathidae         Syngnathus typhle             129           37              135.2          52.6
Cottidae           Taurulus bubalis              7           7              204.8         120.6
Gadidae            Trisopterus esmarkii            5           1               6.0          0.5
Zoarcidae           Zoarces viviparus             82           57             1648.0         474.5
                                    4503          2009            21,877.5         9503.7



Z. marina beds compared to catches from areas where seagrass            between day and night samplings. Furthermore, of the two
had disappeared when sites were compared in pairs. However,            habitat types, Z. marina sites were more closely clustered in
overall no significant difference in fish density could be de-            the analysis than bare sediment sites, indicating a higher sim-
tected between habitats or between day and night samplings             ilarity of the fish assemblages in Z. marina beds.
(Table 3). Except for one sample in the Z. marina bed at loca-             An SIMPER-analysis revealed that the distribution of 10
     ˚ ¨
tion 4 (Gaso), the fish biomass was generally low during day-            species explained about 70% of dissimilarity between the two
time sampling, especially at non-seagrass sites (Fig. 2). Night          habitat types (Table 4). Of these species, eight had higher den-
fish biomass was generally higher than daytime biomass, and             sities in Zostera marina beds and two were more abundant in
similar total fish weights were recorded in the two habitat             non-seagrass habitats. The high affinity of several fish species
types. Overall, a trend toward higher fish biomass was re-             to the Zostera habitat is further emphasised by the fact that
corded in Z. marina beds, although the difference from non-            10 out of the 20 most abundant fish species were almost exclu-
seagrass sites was not significant ( p ¼ 0.10; Table 3).              sively caught in the seagrass beds. Gadoids (Gadus morhua,
  MDS ordination based on a BrayeCurtis similarity matrix             Merlangius merlangus and Pollachius virens) labrids (Cteno-
showed that the fish assemblages were mainly structured ac-             labrus rupestris and Symphodus melops), syngnathids (Syngna-
cording to habitat type, whereas time of the day was of less            thus acus and Entelurus aequoreus) and Gobiusculus flavescens
importance for the structure of the fish assemblages (Fig. 3).           were predominantly found in Z. marina beds, whereas flatfishes
An ANOSIM-test revealed a significant difference (Global              such as Pleuronectes platessa, Platichthys flesus and Solea
R ¼ 0.37; p ¼ 0.01) between the fish assemblage structure in            solea mainly occurred on bottoms dominated by bare sediment.
Zostera marina beds and non-seagrass habitat, but the test               Cod (Gadus morhua) and plaice (Pleuronectes platessa) are
failed to show any difference (Global R ¼ ÿ0.07; p ¼ 0.74)             the most important species of commercial interest that
128                             L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132

                            25  Day
                            20
                            15




                Species per sample
                            10
                            5
                            0
                            25  Night
                            20
                            15
                            10
                            5
                            0

                           1000  Day
                           600
                Numbers per sample




                           200
                            0

                           1400  Night
                           1000
                           600
                           200
                            0


                           8000  Day                     Zostera
                           6000                        Non-Zostera
                Biomass per sample




                           4000
                           2000
                            0
                           8000  Night
                           6000
                           4000
                           2000
                            0
                                   1          2          3              4
                                                 Sites

Fig. 2. Number of species, individuals and biomass of fish captured during day and night samplings at four Zostera marina and four non-Z. marina sites in the
archipelago of the Swedish Skagerrak.


occurred in high densities in this investigation. They both uti-                 1993). From analysis of length distribution it was obvious
lize the coastal zone as a nursery and juveniles may stay in                   that 0-group juvenile cod mainly utilized the Zostera marina
shallow (<10 m) waters for about two years after settlement                    beds as a nursery, whereas 1-group cod were equally repre-
to the benthic habitat (Pihl, 1989; Pihl and Ulmestrand,                     sented in both habitats (Fig. 4). In the Z. marina beds cod

Table 3
Two-fixed-factor ANOVA-modes. Number of species, density and biomass of
fish as a function of habitat (Zostera, no Zostera) and time (day, night)                                              Stress: 0.09
                                                                      2
Source of variation  SS               df   MS       F     p
                                                                          2      1
Number of fish species
                                                                4            4
Habitat        203.1              1   203.1     21.8   0.005                    2  2
                                                            3
Time         39.1               1   39.1      4.2   0.063
Habitat  Time    1.6               1   1.6       0.2   0.692            4
                                                                              1
Residual       111.8              12   9.3                              1
                                                        4
                                                            1
Density of fish
Habitat        388,752             1   388,752     2.58   0.134
Time          133,225             1   133,225     0.88   0.365                      3
Habitat  Time     49,952             1   49,952     0.33   0.575
Residual        1,805,974           12   150,497                Day Night
                                                          Non-Zostera
Biomass of fish                                                   Zostera           3            3
Habitat        9,571,289            1   9,571,289    3.91   0.099
Time          2,051,340            1   2,051,340    0.68   0.424
                                                 Fig. 3. Similarities in fish assemblage structure between day and night
Habitat  Time     2,133,790            1   2,133,790    0.71   0.415
                                                 samplings in four Zostera marina and four non-Z. marina sites, based on
Residual        3.6Eþ07            12   2,996,293
                                                 Multi-Dimensional Scaling (MDS) ordination.
                       L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132              129

Table 4                                      and six species were found in Zostera marina habitats
Fish species most responsible for the difference in assemblage structure be-    (Table 6). Carcinus maenas, Crangon crangon, Palaemon
tween Zostera marina and non-Zostera marina habitats, listed in the order
of their contribution to the average BrayeCurtis dissimilarity. Abundance is
                                          adspersus and Palaemon elegans were the dominant species
mean individuals sampleÿ1                             in both habitats. There was a trend towards higher densities
Rank  Fish species        Abundance         % Contribution
                                          and biomasses in non-seagrass compared to Z. marina sites,
                                          however, the differences were not significant ( p > 0.05).
                  Zostera   Non-Zostera
                                          Catches were higher during the night, with significant larger
1    Aphia minuta        177.8    21.1     11.1         biomass ( p ¼ 0.005) at night compared to day samples in
2    Gasterosteus aculeatus   145.5    114.5      8.4
3    Gobiusculus flavescens    33.0     0       8.2
                                          both habitats.
4    Gadus morhua        18.3     1.5      5.9
5    Gobius niger        92.3    38.0      5.4         4. Discussion
6    Syngnathus typhle      16.1     4.6      5.4
7    Zoarces viviparus      10.3     7.1      5.3           The main purpose of this study was to document shifts in
8    Ctenolabrus rupestris    34.0     0.3      5.0
9    Pleuronectes platessa    2.6    17.9      4.5
                                          the assemblages of fish as a direct consequence of loss of
10   Pomatoschistus minutus    3.8     9.0      4.4         the habitat-forming vegetation, Zostera marina, in shallow
11   Nerophis ophidion      4.0     0.5      3.3         soft-bottom areas. It would be expected that species richness
12   Syngnathus rostellatus    4.1     2.9      3.2         and composition of fish species would change when vegetation
13   Pomatoschistus microps    0     11.3      3.1         disappears as a result of lower habitat complexity (Jackson
14   Syngnathus acus       4.4     0       2.7
15   Pomatoschistus pictus    2.0     2.3      2.6
                                          et al., 2001; Hughes et al., 2002; Lazzari, 2002), but the den-
16   Anguilla anguilla      1.5     2.9      2.5         sity of fish does not necessarily decrease, since shallow soft
17   Platichthys flesus      1.4     4.6      2.5         bottoms are known to host large abundances of small fishes
18   Myoxocephalus scorpius    2.8     0.3      2.5         (Edgar and Shaw, 1995). The archipelago of the area investi-
19   Merlangius merlangus     2.0     0       2.1         gated consists of a mosaic of rocky- and soft-bottom habitats
20   Entelurus aequoreus     2.0     0       2.0
21   Taurulus bubalis       0.9     0.9      1.7
                                          that are to a varying degree covered by vegetation, thereby of-
22   Salmo trutta         1.1     0.5      1.7         fering a suite of alternative habitats with different complexity
23   Clupea harengus       0.1    10.5      1.3         that could be utilized by littoral fish. When seagrass disappears
24   Trisopterus esmarkii     0.6     0.1      0.9         from an area, fish could either concentrate in alternative veg-
25   Pollachius virens      0.5     0       0.7         etated habitats or stay in the altered habitat dominated by
26   Limanda limanda       0.6     0       0.7
27   Symphodus melops       0.5     0       0.7
                                          bare sediment. Therefore, as pointed out in previous studies
28   Nerophis lumbriciformis   0.1     0.1      0.6         comparing fish in seagrass and bare sediment (Ferrell and
29   Pholis gunnellus       0.4     0       0.6         Bell, 1991), it is important to consider the size of the area
30   Spinachia spinachia     0.3     0       0.5         where seagrasses have been lost and the distance to other alter-
31   Solea solea         0      0.1      0.3         native habitats. In our study, the areas where seagrass had dis-
32   Callionymus lyra       0      0.1      0.3
33   Scophthalmus rhombus     0      0.1      0.3
                                          appeared had a size of several hectares and the distance to
                                          vegetated habitats, in this case other seagrass beds or belts
                                          of macroalgae, was between 200 and 500 m. Despite the close
were caught both during day and night, but in the non-seagrass           proximity to complex habitats, a significant reduction in fish
habitats cod only appeared in night samples. In contrast to cod,          species and change in species structure were observed in areas
juvenile 0-group plaice were almost exclusively caught at sites          where seagrass had vanished. Thus, there is a clear indication
dominated by bare sediment (Fig. 5). They occurred on bare             of a shift in the fish assemblage, including a loss of taxa at the
sediment both during day and night. Only a few individuals             family level as a result of degradation in habitat-forming veg-
of 1-group plaice were captured in this study. They appeared            etation at the observed scale.
in both habitats, but were only caught during night sampling.             In our study, fish biomass was generally higher during night
  In an attempt to analyze possible relationships between the           in habitats both with and without Zostera marina. The high
structure of Zostera marina and the fish assemblages (although           biomass was partly due to the larger size of individual fish cap-
based on a small sample size) density, length and biomass of            tured during the night. This indicated that fish migrate into
vegetation were compared to species, density and biomass of            shallow water at night, and these areas may function as
fish (Table 5). Highest number of fish species and biomass              a night-time feeding ground for both types of habitat. Such
was observed in the two Z. marina beds having the greatest             nocturnal shoreward migration has previously been described
blade length and the largest biomass of vegetation. These             for the two dominating commercial species in the area, cod
two beds also had the largest geographical extension of the            and plaice (Pihl, 1982; Gibson et al., 1998). In other investiga-
four investigated Z. marina sites.                         tions it has been shown that fish migrate from seagrass into
                                          open sediment habitats at night for foraging (Gotceitas et al.,
3.4. Macro-crustaceans                               1997).
                                            Different fish species may show different degrees of depen-
  In addition to fish, nine species of macro-crustaceans were           dency on vegetation. Syngnathids is a group of fish species
found in samples from the sites dominated by bare sediment             that are adapted to seagrass by their body shape. The habitat
130                                                   L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132

                                        8
                                             Zostera                          0-group               1-group
                                        7
                                        6
                                        5
                                        4
                         Individuals per length group

                                        3
                                        2
                                        1
                                        0

                                        8
                                             Non-Zostera
                                        7
                                        6
                                        5
                                        4
                                        3
                                        2
                                        1
                                        0
                                          30       40       50     60     70      80   150    200     250      300
                                                            Length, mm                      Length, mm

                   Fig. 4. Number of individuals per length-class of 0- and 1-group juvenile cod (Gadus morhua) at Zostera marina and non-Z. marina sites.


dependence may vary for this group of fishes, but most species                                          fish (Arntz, 1973). In this way, gobies provide an important
are found among vegetation. Six species of syngnathids were                                           energy link from the highly productive shallow coastal system
found in this study, of which four species occurred in both                                           to fish living in deeper less productive water (Moller et al.,
                                                                                                   ¨
habitat types and two species were caught exclusively in Zos-                                          1985). In our study, five species of gobies together contributed
tera marina beds. Altogether, over 80% of the individuals and                                          30% of the numbers and 15% of the biomass of the total fish
biomass of this group of fish were found in the Z. marina. The                                          assemblage at sites dominated by bare sediment. In Zostera
reason that cryptic species like the syngnathids occupy the                                           marina beds, the corresponding figures for gobies were 55
bare sediment habitat is probably because the missing Zostera                                          and 45%, respectively. The total density of gobies was four
beds had partly been replaced by Fucus spp. that could give                                           times higher in Z. marina beds compared to non-seagrass sites,
sufficient camouflage for these fishes.                                                      and biomass was more than six times higher. Thus, Z. marina
  Gobies are important components in the food web of littoral                                         beds seem to have a considerably higher capacity for produc-
fish assemblages, occurring in vegetated as well as unvege-                                           tion of gobies that provides an essential energy transfer link to
tated habitats. They are typically small-sized fish with a short                                         fish during the winter season of low productivity.
life span and high production (Fonds, 1973). In temperate                                             Some fish species may vary in their utilization of habitats
waters, gobies utilize shallow water for growth during the                                           over different time scales. The affinity to vegetation may
summer, but usually migrate to deeper water in wintertime                                            change during ontogeny, as for example, early stages of juve-
where they comprise an important food resource for demersal                                           nile cod are more habitat-specific and remain stationary in
                                                                        vegetation compared to older juveniles (Borg et al., 1997).
                                                                        Cod uses Z. marina beds as a nursery ground and immigrate
                35
                30                                                       to these coastal habitats by larval transport. Juveniles settle
                25                                       Non-Zostera           in the seagrass by active selection usually avoiding open
                20                                                       bare sediment, and consequently the availability of seagrass
Individuals per length-group




                15
                10
                                                                        beds may be considered as a bottleneck in the recruitment pro-
                 5                                                       cess due to the specific habitat requirement of the early benthic
                 0

                35                                                       Table 5
                30
                                                        Zostera
                                                                        Density (individual mÿ2), length (cm) and biomass (g wet wt. mÿ2) of Zostera
                25
                                                                        marina blades (n ¼ 3), and number of species, density (individuals sampleÿ1)
                20
                15
                                                                        and biomass (g wet wt. sampleÿ1) of fish (n ¼ 2) at four Z. marina sites
                10                                                       Zostera marina  Zostera             Fish
                 5                                                       sites
                 0                                                                Density  Length  Biomass    Species  Density  Biomass
                    20  30     40             50  60  70     80  90  100 110 120 130
                                                                        Brofjorden    230    47    172      21     463    1937
                                             Length, mm                      Lindholmen    100    30    44      20     785    1086
                                                                        Finnsbo     380    22    71      20     207    1133
Fig. 5. Number of individuals per length-class of juvenile plaice (Pleuronectes
                                                                         ˚ ¨
                                                                        Gaso       250    40    141      24     797    2260
platessa) at Zostera marina and non-Z. marina sites.
                     L. Pihl et al. / Estuarine, Coastal and Shelf Science 67 (2006) 123e132                    131

Table 6                                      This investigation included areas with different characteris-
Density (individuals sampleÿ1) and biomass (g wet wt. sampleÿ1) of macro-   tics in terms of exposure, sediment type and vegetation struc-
crustaceans at Zostera marina and non-Zostera marina sites during day and
night samplings
                                        ture. However, organic content of the sediment, as well as
                                        Zostera shoot density, blade length and biomass, of the studied
Sites          Zostera marina     Non-Zostera marina
                                        Zostera marina beds in 2004 were within the range of what has
            Day     Night    Day      Night      previously (1982e1990) been reported for the Swedish coastal
Density                                    region (Baden and Pihl, 1984; Baden and Bostrom, 2001).
                                                                   ¨
Athanas nitescens                 0.8      1.3      Thus, there are no indications that the characteristics of the ex-
Carcinus maenas     11.3    24.0    29.8      26.8
Crangon crangon     11.3    33.3    53.3     171.8
                                        tant Z. marina meadows have changed over the last two dec-
Gammaridae        0.0     0.0     1.5      1.3      ades. The number of species and density of fish recorded in
Macropodia rostrata   20.0    12.8     0.3      2.5      this study are also in accordance with what have previously
Mysidae          0.3     0.0     9.3      1.5      been found in surveys of Z. marina beds on the Swedish Ska-
Palaemon adspersus    24.0    134.3    155.8     236.0      gerrak coast. Investigations carried out during June between
Palaemon elegans     17.0    75.8    113.3      86.3
Pagurus bernhardus    0.0     0.0     0.5      0.0
                                        2000 and 2004, including 18 Z. marina beds from three costal
                                        regions of the Swedish west coast, estimated number of spe-
Total density      83.8    280.0    364.3     527.3
                                        cies and densities of fish per standard haul to 14.3 and 643, re-
Biomass          0.0     0.0            0.0      spectively (Anders Svenson, personal communication). The
Athanas nitescens     0.0     0.0     0.1      0.3      corresponding figures for number of species and density of
Carcinus maenas     62.0    339.5    120.3     254.0      fish in the present study was 16.2 and 389, respectively. There-
Crangon crangon      6.3    17.8    22.8      76.5      fore, the result from this study concerning both vegetation and
Gammaridae        0.0     0.0     0.1      0.1
                                        fish could be considered representative for Z. marina beds in
Macropodia rostrata   14.8     7.8     0.1      2.8
Mysidae          0.0     0.0     0.7      0.3      the archipelago, and the findings would be expected to be gen-
Palaemon adspersus    12.7    64.5    57.4     153.6      erally applicable for the Swedish west coast.
Palaemon elegans     6.0    45.1    45.3      49.5
Pagurus bernhardus    0.0     0.0     1.0      0.0
Total biomass      101.8    474.6    247.6     536.9      Acknowledgments

                                         This project is a part of the research program MARBIPP
stages. Other gadoids, such as Merlangius merlangus and Pol-          (Marine Biodiversity: Patterns and Processes) funded by the
lachius virens, may also use vegetated coastal habitats as nurs-        Swedish Environmental Protection Agency, which are kindly
ery grounds, and in our study juvenile of these two species          acknowledged. We also thank Andreas Wikstrom for valuable
                                                               ¨
were exclusively found in Z. marina beds. Thus, Z. marina           assistance during field sampling.
beds are essential habitats during the recruitment process for
gadoids, and losses of seagrass will most likely reduce the
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