Overgrowth patterns of the red algae Furcellaria lumbricalis at an exposed Baltic Sea coast: The results of a remote underwater video data analysis

Estuarine, Coastal and Shelf Science 75 (2007) 308e316 www.elsevier.com/locate/ecss

Overgrowth patterns of the red algae Furcellaria lumbricalis at an exposed Baltic Sea coast: The results of a remote underwater video data analysis Martynas Bucas*, Darius Daunys, Sergej Olenin Coastal Research and Planning Institute, Klaip_eda University, H. Manto 84, LT 92294 Klaip_eda, Lithuania Received 12 December 2006; accepted 30 April 2007 Available online 6 August 2007

Abstract The exposed coast on the tide-less south-eastern Baltic Sea is generally unsuitable for large perennial, habitat forming plants, such as eelgrass and bladder wrack. In this area the dominant perennial macrophyte, Furcellaria lumbricalis, provides an important substrate for the eggs of commercial fish. This algae is limited to the hard substrates and abundant at depths of 6e10 m. However, the distribution of F. lumbricalis is patchy, probably due to the effects of exposure and abrasion from mobile sediments. It has been proposed that the extent of F. lumbricalis cover relates to substrate size and stability, sediment abrasion, depth and the direction of predominant stormy winds. A remote underwater video equipment was used to obtain records of distribution of these algae. Video footage was segmented into still images from where physical and biological parameters were obtained. F. lumbricalis occurred on cobbles, boulders, and occasionally on pebbles. Cover of algae was greater on boulders surrounded by a stable bottom (boulders) than surrounded by sands and gravels. Cover on cobbles was similar on all bottom types probably due to the movement of this substrate during storms. F. lumbricalis occurred close to the seabed on those substrates on stable bottoms where compared with mobile ones. However, elevation of algae from the seabed and cover patterns depended on depth. According to direction of wind exposure, cover on substrates was greater on sheltered surfaces in comparison to exposed ones, where the F. lumbricalis was dislodged during storms. The distribution of cover of F. lumbricalis may alter according to storm frequency as predicted to take place with changes in climate. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: phytobenthos; patchiness; sediment stability; abrasion; wind exposure; sublittoral

1. Introduction The phytobenthos distribution in Baltic Sea is determined by many environmental gradients and their interactions (Wallentinus, 1991; Kautsky, 1995; Kiirikki, 1996; Orav et al., 2004; Eriksson and Bergstro¨m, 2005; Eriksson and Johansson, 2005). The role of these environmental factors varies according to the conditions occurring in different localities in the Baltic Sea. For instance the salinity gradient determines the distribution of marine kelps and fresh water plants

* Corresponding author. E-mail address: [email protected] (M. Bucas). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.04.038

(phanerogams) which are normally confined to soft sediments (Snoeijs, 1999). Wave exposure and ice scouring generally effect the zonation of brown seaweeds at the northern Baltic Sea regions (Kiirikki, 1996). The exposed south-eastern (SE) Baltic coast is unfavourable for the most widespread habitat forming species, such as eelgrass (Zostera marina L.) and bladder wrack (Fucus vesiculosus L.) (Haage, 1975; Baden and Bostro¨m, 2001) due to active hydrodynamic conditions. The only dominant perennial macrophyte at the SE Baltic coast is the red algae Furcellaria lumbricalis (Huds.) Lamour which is known to be an important commercial species and a spawning substrate for fish (Kireeva, 1960a,b; Trei, 1984; Olenin and Labanauskas, 1994; Korolev and Fetter, 2003; Andrulewicz et al., 2004). This species is

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widely distributed in the northern hemisphere: Atlantic and Indian Oceans, Mediterranean and Baltic Seas (Guiry, 2006). Earlier studies have shown that at the SE Baltic Sea coast, Furcellaria lumbricalis is generally limited by the availability of light and hard substrates (Blinova and Tolstikova, 1972; Labanauskas, 1998). The species occurs from ca. 3 to 16 m, and is abundant in its optimal depth range from ca. 6 to 10 m (Kireeva, 1960b; Olenin et al., 2003). In more sheltered waters of other eastern Baltic regions, F. lumbricalis grows at depths up to 1 m (Wallentinus, 1979; Martin, 1999), indicating that the wave effect may be a limiting factor on exposed coasts. The distribution of Furcellaria lumbricalis is patchy even within its optimal depth range varying in abundance from single specimen to very dense beds (Olenin and Labanauskas, 1994; Olenin et al., 2003). Size and stability of substrates as well as the surrounding bottom (on which these substrates are situated) are also very diverse within this depth zone. Therefore, it has been suggested that the distribution patterns of F. lumbricalis relate to substrate size, exposure to stormy winds and abrasion by mobile sediments. Since direct observations at the exposed coast are seldom possible, a remote underwater video survey was undertaken. This method allowed mapping of small-scale distribution of algae which may reflect the consequences of abrasion and storm effects. The following working hypotheses were formulated:

309

 the cover of F. lumbricalis should be greater on large and stable substrates (e.g. boulders) which help the algae to avoid scouring and detachment;  the cover of the algae should be greater on substrates surrounded by stable sediments (e.g. boulders) than on substrates surrounded by mobile sediments (e.g. sands and gravels);  the position of F. lumbricalis holdfast on the substrate should be higher above the seabed surrounded by mobile sediments than by stable sediments, due to abrasion effect;  the substrate mobility and effect of sediment abrasion upon the cover of algae should be greater at lower depths than at deeper sites; and  the cover of F. lumbricalis should be denser on sheltered surfaces of substrates (in case of this study site: E, NE and SE) compared to exposed ones (W, NW and SW).

2. Methods 2.1. Study area The underwater study area was on the south-eastern part of the Baltic Sea coast, Lithuania, where abundant Furcellaria lumbricalis beds occur (Fig. 1) (Blinova and Tolstikova, 1972;

Fig. 1. Study site and location of video transects within the Furcellaria lumbricalis bed at the Lithuanian coast, SE Baltic Sea.

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Olenin and Labanauskas, 1994; Olenin et al., 2003). The coast is exposed with a wave fetch of >200 km from any westerly direction. To the east is the shore in ca. 0.5e8 km. Waves are wind-induced with a mean height of w2 m. The highest measurements were of 6.7 m, while in conditions of extreme storms (wind > 30 m s1) modelled waves attained 12 m (Zˇaromskis, 1982; Asˇmontas, 1994). Near the bottom, currents range from 5 cm s1 to 50 cm s1 due to a heterogeneous bottom topography, speed and direction of winds (Dubra, 1994). The underwater slope (15e45 km width, down to ca. 30 m isobath) is characterized by glacial deposits (morainic clay), large boulders, cobbles, pebbles, gravel and sand (Gulbinskas and Trimonis, 1999). Sediment distribution is determined by the sedimentation of the material transported from the Curonian Lagoon, as well as abrasiveeerosive processes (Gudelis and Janukonis, 1977; Zˇaromskis, 1992). Generally, the sediment is transported northwards along the shore. During strong storms, the wind usually varies from the SW to NW directions, which alters the direction of sediment transport. This can include pebble transport (Zˇaromskis, 1994). 2.2. Field methods A towed underwater video array was used for the field survey during June 2003. The array was towed on a 20-m long tether behind a 6-m vessel. Sensors were high-resolution (530 lines) cameras (SONY TRV-DCR 950 Mini DV and C-Tecnics Subsea Video 302), mounted in a housing at ca. 45 angle to the bottom. Two laser diodes projected two dots onto the bottom at a constant distance of 10 cm one from another. This laser scale enabled an estimation of the

spatial resolution of video images, position and size of organisms. A depth sensor was mounted in the housing, where the signal was overlayed and recorded in each video frame. Video transects were randomly chosen within the depth range of 6e12 m. The sea bottom was continuously recorded while drifting within ca. 100e150 m long transects. Start and end points of transect were located using GPS (M12 OncoreÔ; with a positioning accuracy of less than 25 m), from which route and direction of the array were determined. In total, 11 video transects were made.

2.3. Video analysis Since there are a small number of publications on methodology for underwater video processing and quanitative analysis (Davies et al., 2001), our own method was developed in this study. The video footage was captured in AVI format and segmented into still images (frames) in JPG format using VirtualDub software (www.virtualdub.org, verified November 2005). The images, containing the same information (overlapping frames) and poorly recognizable physical and biological features were not used. Selected frames were treated as random samples from the video transect, and analysed by eye. Differences of zoom in the images ranged from 400 to 2100 cm2 of the visible seabed surface area. If a selected frame had closer zoom to a bottom or some unclear objects, neighbouring frames were repeatedly studied and data of the selected still image were reanalysed and/or corrected. Five physical and four biological parameters were derived from every sample (Table 1 and Fig. 2). Not all images were

Table 1 List of parameters derived from the video analysis Parameter name and abbreviation

Description

No. of samples

Depth Type of substrate

Measured from the depth sensor; m Sediments on which Furcellaria lumbricalis occurred; classified according to Wentworth scale (Wentworth, 1922) Sediments around the substrates; classified according to Wentworth scale Mobile (sand, granules/gravel, pebbles, cobbles) Stable (small and large boulders) Mobile (>70% sand, gravel, pebbles, cobbles) Stable (>70% small and large boulders) Intermediate (w50% mobile and w50% stable bottom types) Percentage of algae cover measured in five ordinal classes on individual types of substrates: 0 (absence of algae) 1 (single bushes, <20% area of substrate) 2 (solitary groups, 20e50%) 3 (moderate overgrowth, 50e80%) 4 (entire overgrowth, >80%) Evaluated as weighted average of algae cover on all types of substrates in an image; same units as in the CFS Measured perpendicularly from the seabed to a lowest attached holdfast of algae on substrate; cm The cover measured on the surfaces of substrates divided by the four cardinal and four half-cardinal points of the compass: N, NE, E, SE, S, SW, W, NW; same units as in the CFS

1025 1025

Type of surrounding bottom sediments (SBS) Mobility of substratea Mobility of surrounding bottom sediments (MSBS)

Cover of Furcellaria lumbricalis on substrates (CFS)

Total cover of F. lumbricalis (TCF) Minimum distance between the seabed and holdfast of F. lumbricalis on substrate (MDSF) Cover of F. lumbricalis on substrate surfaces of different orientation (CFSDO) a

According to Connor et al. (2004) and Osborne (2005), see text for details.

1025 1025 1025

939

1025 1025 672

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311

N

W

E E

S 10 cm

10 cm

MDFS

10 cm

10 cm

Fig. 2. Examples of the estimation of biological parameters (see Table 1) from the still images. The CFS: class 1 on cobble (upper left image), class 2 on small boulder (upper right image), class 3 on large boulder (lower left image), class 4 on small boulders (lower right image). The MDSF measured as the minimum distance between the seabed and the lowest holdfast of the algae on substrate (lower left image): ca. 35 cm. The CFSDO measured by the eight points of the compass (upper right image), the cover is 2, 3, 2 on the NE, E, SE surfaces, respectively, and 0 on other surfaces of substrate.

suitable for deriving all the parameters, therefore, the number of frames for parameters was different. In this study bottom sediments were characterized using two parameters: types of substrate and surrounding bottom sediments (SBS) (Table 1). Both parameters were also classified by sediment mobility. The sediment classes from sand to cobbles were considered to be mobile substrates under storm conditions, while boulders were considered stable. Mobility of SBS was classified by the stability of the predominant sediment class. Where small and large boulders comprised >70% of sediment on the seabed, the SBS was considered stable. In cases where the seabed consisted of >70% of mobile sediments, the SBS was determined mobile. The intermediate SBS was represented by equal surface areas of mobile and stable SBS. The cover of Furcellaria lumbricalis on substrates (CFS) was evaluated for each class of substrate (Fig. 2). Certain sediment classes did not occur in each depth interval, thus the CFS parameter could not be estimated within the whole depth gradient. Therefore the CFS was averaged for all substrate classes and a further parameter (TCF) was included in the analysis, to reflect the changes of the total algae cover along the depth gradient. 2.4. Additional data and statistical methods Two-way analysis of variance (ANOVA) and Tukey’s studentized range test were used to verify the hypotheses (Quinn

and Keough, 2002). The data were tested for adherence to assumptions of variance equality and normality by using scatterplots and distribution fitting (Zuur et al., 2007). Diagnostic tools for distribution of dependent variable, studentized residuals, normal probability plots as well as correlation between mean and standard deviation (S.D.) were also used in ANOVA models (StatSoft Inc., 2006). In cases where the assumptions were not met, transformations were applied: the CFS data were divided by S.D. of the groups, whereas the MDSF data were log transformed. The parameter of frequency of stormy winds (speed of 10 m s1) in four cardinal and four half-cardinal points of the compass (data for the period 2000e2003 obtained from the Lithuanian Hydrometeorological Service) was used for analysis of effect of storms on Furcellaria lumbricalis cover on substrate. Spearman’s rank correlation was used for the determination of relationship between categorical variables: frequency of stormy winds and the CFSDO. Means and standard deviations were used in the study to represent the estimated parameters and their variability. 3. Results The substrates, suitable for the red alga Furcellaria lumbricalis were pebbles, cobbles, small and large boulders. The surrounding bottom sediments (SBS) included also sands and gravel besides the substrates listed above. Where the cover of algae was dense the underlying substrate often could not

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312

F. lumbricalis cover (CFS), classes

4

3

Mobility of SBS: stable intermediate mobile

a ab

ba ba 2 b b

b b

b

1

0 cobbles (mobile)

small boulders (stable) large boulders (stable)

Type of substrate Fig. 3. The mean cover of F. lumbricalis on different substrate (CFS) types within mobile, intermediate and stable surrounding bottom sediments (SBS). The letters indicate homogenous groups of Tukey’s HSD test (N ¼ 90, Mean  0.95 Conf. intervals). Data transformed by S.D. of the groups.

be determined. This mainly occurred in cases of algae overgrowth on pebbles therefore this substrate type was excluded from the analysis of the species cover. The mean cover of Furcellaria lumbricalis on substrates (CFS) significantly differed between the substrate types (Fig. 3, Table 2). Cobbles were the least suitable substrate where the mean algal cover was low within all mobility types of surrounding bottom sediments (MSBS): 0.3  1.0, 1.0  1.0, 0.7  1.0 on the mobile, intermediate and stable SBS, respectively. The maximum CFS (average 2.7  1.0) determined on large boulders, however, was not significantly different from the cover on small boulders (average 2.4  1.0). Table 2 Results of two-way ANOVA mixed models (bold P values indicate significant factors) MS

F

P

2 2 4 81

6.768 17.994 2.78 0.994

6.810 18.106 2.80

<0.001 <0.001 <0.05

TCFS MSBS Depth MSBS  depth Residual

4 1 10 176

6.713 22.513 3.650 0.745

9.007 30.205 4.897

<0.001 <0.001 <0.001

MDSF MSBS Depth MSBS  depth Residual

4 1 10 176

0.267 0.02 0.554 0.066

4.066 0.33 8.452

<0.01 >0.05 <0.001

CFSDO Orientation of substrate surface Depth CFS  depth Residual

7 5 35 624

4.92 12.276 1.80 1.473

3.34 8.332 1.22

<0.01 <0.001 >0.05

Sources of variation CFS Substrate MSBS Substrate  MSBS Residual

d.f.

The CFS on the stable SBS was the highest, followed by the intermediate and mobile SBS (Table 2). In general the density of total cover of Furcellaria lumbricalis (TCF) on the stable and intermediate SBS increased from 6 to 9 m, and decreased from 9 m (Fig. 4). On the mobile SBS, the cover values were low (average 0.3  0.8) and displayed no particular pattern along the whole depth gradient. The TCF was twice as dense on the stable SBS (average 2.3  1.2) where compared with the intermediate SBS in the range of 6e9 m depth. On both types of SBS, however, the highest mean values of TFC were reached at 9 m depth (4.0  0.0 on stable and 1.7  1.3 on intermediate SBS) and were consistently low at greater depths. Furcellaria lumbricalis on the substrates occurred in a distance of 3e50 cm above the seabed, however, different patterns of algae position were found on various types of SBS (Fig. 5). On stable SBS the minimum distance between the seabed and the holdfast of F. lumbricalis on substrate (MDSF) was similar at 6e9 m (average 5  1 cm) and was significantly greater below 10 m depth (30  0 cm). On the intermediate SBS, this was constant at 6e10 m (6  2 cm), and reached 25  7 cm at greater depths (Table 2, Fig. 5). On the mobile SBS, the algae occurred 14  11 cm at depths of 7e8 m, whereas below 10 m the MDSF was significantly lower (6  6 cm). In general, the differences in the MDSF between bottoms of different mobility were more pronounced at depth below 9 m, whereas those within the depth range 6e9 m the MDSF were relatively similar on all the SBS. The mean cover of Furcellaria lumbricalis was significantly greater on sheltered surfaces (E and NE) of substrates than on the exposed surface (W) (Table 2, Fig. 6). The largest mean cover of the algae was the same on the NE and E surfaces (1.8  1.3), with least on western facing surfaces (1.1  1.2). The frequency of stormy winds affected the exposed western surfaces of substrates (Fig. 6). Significant negative relationship (r ¼ 0.97, P < 0.05) was determined between the mean cover of Furcellaria lumbricalis on substrate surfaces of different orientation (CFSDO) and frequency of stormy winds. The algal cover was lower on the exposed western surfaces of the substrate, facing predominant stormy wind directions, where compared to the sheltered eastern surfaces. 4. Discussion The importance of hydrodynamics is evident for the survival and spatial distributions of coastal marine macrophytes (Ronnberg and Lax, 1980; Hurd et al., 1996; Denny et al., 1997; Underwood and Chapman, 1998; Ruuskanen and Back, 1999; Cole et al., 2001; Goldberg and Kendrick, 2004). Several studies have shown how the water flow results in pruning and dislodgement of algae (Bell, 1999; Denny and Gaylord, 2002; Malm et al., 2003; Thomsen et al., 2004; Thomsen and Thomas, 2005). However, the abrasion effect of mobile sediments on phytobenthos distribution has seldom been addressed (Sanderson, 1957; Austin, 1960b).

M. Bucas et al. / Estuarine, Coastal and Shelf Science 75 (2007) 308e316 a F. lumbricalis cover (TCF), classes

a

Mobility of SBS: stable intermediate mobile

a

4 a

NW

3 ab

b

2 b

b 1

b

b b

b

b

b bc

b

b

6 5 4 3 2

313

N

rose of F. lumbricalis cover rose of stormy winds NE

1 0

W

E

b

bc

0 SW

SE

-1 S 6

7

8

9

10

11

12

Depth, m

Fig. 6. Mean annual frequencies of stormy winds and the mean cover of F. lumbricalis on substrate surfaces of different orientation (CFSDO).

Fig. 4. The TCF on different types of surrounding bottom sediments (SBS) along the depth gradient (N ¼ 195, Mean  0.95 Conf. intervals). The letters indicate homogenous groups according to Tukey’s HSD test. Mobile SBS were not observed at 6 and 10 m depth.

This study concentrated on small scale (tens of centimeters to meters) distribution patterns of the red algae Furcellaria lumbricalis on the exposed coast. At this scale, the cover of algae depended on the properties of the substrate and surrounding seabed. Few algae were attached to pebbles and cobbles, and cover of F. lumbricalis was the most dense on small and large boulders. Pebbles and cobbles are probably too small to hold the algae sufficiently high above the seabed to avoid sediment abrasion and also may become unstable during storms and damage the algae. Cover was significantly greater where the substrates were surrounded by stable bottom (boulders), than where surrounded by mobile one (sand, gravel, pebbles and cobbles). These results support the sediment mobility classes categorized by the biotope classification (Connor et al., 2004).

Distance (MDFS), cm

40

30

a

Mobility of SBS: Stable Intermediate Mobile

a

a

a a a

20 abab

a abab

ab ab

10

b

ab

b b

ab b

0

-10 6

7

8

9

10

11

12

Depth, m Fig. 5. The MDSF on different types of surrounding bottom sediments (SBS) along the depth gradient (N ¼ 195, Mean  0.95 Conf. intervals). The letters indicate homogenous groups according to Tukey’s HSD test. Mobile SBS were not observed at 6 and 10 m depth.

The importance of sediment abrasion was revealed by the analysis of the minimum distance between the seabed and holdfast of Furcellaria lumbricalis on substrate (MDFS). On the mobile bottom, the algae were attached to the substrate at a distance several times greater than on the stable bottom. This pattern, however, was clear in depths down to 9 m. In the deeper zone, the MDFS increased and the total cover of F. lumbricalis (TCFS) sharply decreased (Figs. 4 and 5), most probably due to decrease in light availability. Such declines of the species biomass with depth were also found in the SE Baltic earlier (Kireeva, 1960b). She also noticed depth related differences in morphology of F. lumbricalis tufts. The algal bushes were broader, thicker, more regularly dichotomised and formed sparser colonies at depths greater than 10 m. Frequent irregular branching of F. lumbricalis was explained by the damaging effect of waves in the shallower waters (Kireeva, 1960b). The effect of storms on Furcellaria lumbricalis for this region is evident from the drifts of algae accumulating on shores (Kireeva, 1960a; Orlov, 1965; Blinova, 1971; Korolev et al., 1983). Greater quantities of algae were stranded following western storms. In this study the denser cover of algae on the eastern sheltered surfaces of substrates also demonstrated the impact of storms, however, this effect was not found in areas with mobile sediments adjacent to the substrate. Temperature, salinity and nutrients are also important for the distribution of phytobenthos (Wallentinus, 1991; Kautsky, 1995; Snoeijs, 1999), however, these factors seldom change at a small scale and therefore are not responsible for the variations in the cover of Furcellaria lumbricalis. Scouring by ice does not take place in this region of the Baltic Sea and is not important for the species distribution. Grazing, overgrowth by epibionts and competition for space are also known to influence the structure of macrophyte communities (Worm et al., 1999; Lotze et al., 2001; Lotze and Worm, 2002; Berger et al., 2003). In the eastern part of the Baltic Sea grazing by the isopod Idotea baltica (P.) has been investigated by Kotta et al. (2000), Orav-Kotta and Kotta (2004) and Orav et al. (2004) and these studies showed that this isopod used

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algae principally for shelter. The significant effect of I. baltica on Fucus vesiculosus was found at much higher abundance of isopod (1073  1517 individuals per 100 g wet weight of algae) (Kangas et al., 1982) than in our study area (5  5 individuals per 100 g wet weight of Furcellaria lumbricalis) (Olenin et al., 2003). Padilla (1993) showed that active hydrodynamics can reduce the number of grazers. We concluded that this isopod had no significant grazing effect on F. lumbricalis. In the northern Baltic epibionts can limit the growth of Fucus vesiculosus by shading (Kangas et al., 1982). In the south-eastern Baltic, epibionts on Furcellaria lumbricalis include the filamentous red algae (Ceramium spp., Polysiphonia and Rhodomela spp.), blue mussels (Mytilus edulis L.) and bryozoans (Electra crustulenta P.) (Blinova and Tolstikova, 1972; Labanauskas, 1998). Their greatest abundance occurred where there were dense overgrowths of F. lumbricalis, indicating the negligible role of the shading by epibionts to the species distribution. Other studies have shown that epibionts can increase frictional resistance provoking easier dislodgement of F. lumbricalis by water movements (Austin, 1960a) and this effect may be enhanced during storms. Potential competitors for space in the south-eastern Baltic Sea include filamentous algae Cladophora spp., Pilayella littoralis (L.) K., Ectocarpus siliculosus (D.) L., Sphacelaria arctica H., Ceramium spp., Polysiphonia and Rhodomela spp., and mussels Mytilus edulis, bryozoans Electra crustulenta, hydrozoans Cordylophora caspia P., and barnacles Balanus improvisus D. In most cases the filamentous algae occurred on both mobile and stable substrates where the Furcellaria lumbricalis obviously did not occur. Olenin et al. (2003) found higher densities of mussels on vertical surfaces of boulders and cobbles in comparison to the horizontal surfaces on the upper part of these substrates. There may be competition between the algae and mussels on the uppermost surfaces within the optimal depth range for F. lumbricalis. Bryozoans, hydrozoans and barnacles were infrequent and unlikely to have impact. Furcellaria lumbricalis reproduces through spores and gametes released synchronously during winter and early spring (Austin, 1960a; Bird et al., 1991). The spores need to attach directly to the substrate (Austin, 1960b), and so hydrometeorological conditions and substrate availability are important for settlement. Although displacement by epilithic organisms, grazing and/or filtration of spores by suspension feeders may impact the recruitment (Norton, 1992), no such studies are known to have taken place in the Baltic Sea. Summarizing results, four key factors are distinguished to explain the distribution Furcellaria lumbricalis at an exposed coast: depth, type of substrate, frequency of storms and mobility of surrounding bottom. Depth and type of substrate primarily determine the species occurrence on the seabed. Both factors explain large scale pattern of the species distribution (hundreds of meters to kilometers) along the underwater slope restricting the species distribution mostly to cobbles and boulders in depths down to 15 m. There is only narrow depth range below 4 m where the storms and mobility of surrounding bottom are preventing the species colonization on suitable substrates.

At the small scale (centimeters to meters) the species distribution patterns are reflected in the cover and position of the algae on substrates. Frequency of stormy winds and mobility of surrounding bottom are two factors playing the major role here, however, their effects are changing with the depth and type of substrate. Results showed that surfaces of substrate oriented at directions of more frequent storms are less covered by algae in comparison to surfaces exposed to storms of lower frequency. Since strong stormy winds occur basically from all directions, frequency of storms rather than a single storm event is important in shaping the algae distribution on the substrate. Additionally, position of the algae on substrate is also adjusted by type of surrounding bottom. Mobile sediments around the substrate reduce the potential surface for growth of algae by scouring and/or preventing colonization. Therefore higher cover of algae occurs on substrates situated on the seabed of lower mobility. The role of surrounding sediments seems to be also dependent on frequency of storms, which may affect an extent of sediment transport. The results of this study imply that the destructive effect of waves and sediment abrasion amplified by the climate change may cause a decline in the abundance of habitat forming algae at the exposed coast. This study shows the effects of principal factors, which determine the species cover and its position on the substrate at the exposed coast. However, thresholds in hydrodynamic characteristics remain not quantified and could be more thoroughly tested using flume systems or properly designed field experiments. Further studies should also address the questions of mechanisms involved in limitation of the species distribution during different life stages.

Acknowledgments This research was funded by EU FW 5 BioFlow (EVR1CT-2001-20008) and MarBEF (GOCE-CT-2003-505446). We would like to thank Dan Minchin, Anna Olenina, Saulius Bucas and Angelija Bucien_e for their comments on the manuscript and the Lithuanian Hydrometeorological Service for access to the meteorological data.

References Andrulewicz, E., Kruk-Dowgiallo, L., Osowiecki, A., 2004. Phytobenthos and macrozoobenthos of the Slupsk Bank stony reefs, Baltic Sea. Hydrobiologia 514, 163e170. Austin, A.P., 1960a. Life history and reproduction of Furcellaria fastigiata (L.) Lamouroux. Annals of Botany New Series 24, 257e274. Austin, A.P., 1960b. Observations on the growth, fruiting and longevity of Furcellaria fastigiata (L.) Lamouroux. Hydrobiologia 15, 193e207. Asˇmontas, A., 1994. Climate and hydrometeorological regime. In: Lazauskas, J. (Ed.), Oil Terminal in Buting_e. Baltic ECO, Vilnius, pp. 54e70 (in Lithuanian). Baden, S., Bostro¨m, C., 2001. The leaf canopy of seagrass beds: faunal community structure and function in a salinity gradient along the Swedish coast. Ecological Studies 151, 214e236. Bell, E.C., 1999. Applying flow tank measurements to the surf zone: predicting dislodgment of the Gigartinaceae. Phycological Research 47, 159e166.

M. Bucas et al. / Estuarine, Coastal and Shelf Science 75 (2007) 308e316 Berger, R., Henriksson, E., Kautsky, L., Malm, T., 2003. Effects of filamentous algae and deposit matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea. Aquatic Ecology 37, 1e11. Bird, C.J., Saunders, G.W., McLachlan, J., 1991. Biology of Furcellaria lumbricalis (Hudson) Lamouroux (Rhodophyta: Gigartinales), a commercial carrageenophyte. Journal of Applied Phycology 3, 61e82. Blinova, E.I., Tolstikova, N.E., 1972. Stocks of commercial agar-reach algae Furcellaria fastigiata (Huds.) J.V. Lamour. in the coast of Lithuania. Rastitel’nye Resursy 8 (3), 380e388 (in Russian). Blinova, E.I., 1971. Size and dynamics of casted Furcellaria lumbricalis ashore in the Baltic Sea. Rybovodstvo 7, 10e11 (in Russian). Cole, R.G., Babcock, R.C., Travers, V., Creese, R.G., 2001. Distributional expansion of Carpophyllum flexuosum onto wave-exposed reefs in northeastern New Zealand. New Zealand Journal of Marine and Freshwater Research 35, 17e32. Connor, D.W., Allen, J.H., Golding, N., Howell, K.L., Lieberknecht, L.M., Northen, K.O., Reker, R.K., 2004. The Marine Habitat Classification for Britain and Ireland Version 04.05. JNCC, Peterborough, ISBN 1 861 07561 8. Available from: . Davies, J., Baxter, J., Bradley, M., Connor, D., Khan, J., Murray, E., Sanderson, W., Turnbull, C., Vincent, M., 2001. Marine Monitoring Handbook, 405 pp. Denny, M.W., Gaylord, B.P., Cowen, E., 1997. Flow and flexibility II: the roles of size and shape in determining wave forces on the bull kelp, Nereocystis luetkeana. Journal of Experimental Biology 200, 3165e3183. Denny, M., Gaylord, B., 2002. The mechanics of wave-swept algae. The Journal of Experimental Biology 205, 1355e1362. Dubra, J., 1994. Currents’ regime. In: Lazauskas, J. (Ed.), Oil Terminal in B uting_e. Baltic ECO, Vilnius, pp. 54e70 (in Lithuanian). Eriksson, B.K., Johansson, G., 2005. Effects of sedimentation on macroalgae species-specific responses are related to reproductive traits. Oecologia 143, 438e448. Eriksson, B.K., Bergstro¨m, L., 2005. Local distribution patterns of macroalgae in relation to environmental variables in the northern Baltic Proper. Estuarine, Coastal and Shelf Science 62, 109e117. Goldberg, N.A., Kendrick, G.A., 2004. Effects of island groups, depth, and exposure to ocean waves on subtidal macroalgal assemblages in the Recherche Archipelago, Western Australia. Journal of Phycology 40, 631e641. Gudelis, V., Janukonis, Z., 1977. Dynamical classification and regionalism of the Baltic Sea coastal zone. Proceedings of Lithuanian SSR Academy of Science B 4 (101), 154e159 (in Lithuanian). Guiry, M.D., 2006. AlgaeBase Version 4.1. World-wide electronic publication. National University of Ireland, Galway. Available from: (accessed 04.04.06.). Gulbinskas, S., Trimonis, E., 1999. Lithodinamical processes in the straight of Klaip_eda. Annals of Geography 32, 93e102 (in Lithuanian). Haage, P., 1975. Quantitative investigations of the Baltic Fucus belt macrofauna. 2. Quantitative seasonal fluctations. Contributions from the Asko¨ Laboratory, University of Stockholm 9, 1e88. Hurd, C.L., Harrison, P.J., Druehl, L.D., 1996. Effects of seawater velocity on inorganic nitrogen uptake by morphologically distinct forms of Macrocystis integrifolia from wave-sheltered and exposed sites. Marine Biology 126, 205e214. Kangas, P., Autio, H., Hallfors, G., Luther, H., Niemi, A., Salemaa, H., 1982. A general model of the decline of Fucus vesiculosus at Tvarminne, south coast of Finland in 1977e1981. Acta Botanica Fennica 118, 1e27. Kautsky, H., 1995. Quantative distribution of sublitoral algae and animal communities along the Baltic Sea gradient. Biology and ecology of shallow coastal waters. In: Proceedings of the 28th European Marine Biology Symposium. Olsen & Olsen, Fredensborg, Denmark, pp. 23e30. Kiirikki, M., 1996. Mechanisms affecting macroalgal zonation in the northern Baltic Sea. European Journal of Phycology 31 (3), 225e232. Kireeva, M., 1960a. Quantitative estimation of seaweed discharges in the Baltic Sea. Trudi WNIRO 42, 206e209 (in Russian). Kireeva, M., 1960b. Distribution and biomass of marine algae in the Baltic Sea. Trudi WNIRO 42, 195e205 (in Russian).

315

Korolev, A., Muravsky, V., Prytkov, E., 1983. Discharges of Furcellaria on the shore caused by storms and their basic characteristics in the Baltic Sea. Riga. In: Rybohozjaistvennie issledovanija v basseine Baltijskogo morja, vipusk 18, pp. 95e102 (in Russian). Korolev, A., Fetter, M., 2003. The mapping of biocenoses in the coastal zone of Latvia. ICES CM2000/T, 11 pp. Kotta, J., Paalme, T., Martin, G., Makinen, A., 2000. Major changes in macroalgae community composition affect the food and habitat preference of Idothea baltica. Hydrobiologia 85 (5e6), 697e705. Labanauskas, V., 1998. Diversity and distribution of macroalgae species along the northern part of the Lithuanian Baltic coastline. Botanica Lithuanica 4 (4), 403e413 (in Lithuanian). Lotze, H.K., Worm, B., Sommer, U., 2001. Strong bottom-up and top-down control of early life stages of macroalgae. Limnology and Oceanography 46, 749e757. Lotze, H.K., Worm, B., 2002. Complex interaction of ecological and climatic controls on macroalgal recruitment. Limnology and Oceanography 47, 1734e1741. Malm, T., Kautsky, L., Claesson, T., 2003. The density and survival of Fucus vesiculosus L. (Fucales, Phaeophyta) on different bedrock types on a Baltic Sea moraine coast. Botanica Marina 46 (3), 256e262. Martin, G., 1999. Distribution of phytobenthos biomass in the Gulf of Riga (1984e1991). Hydrobiologia 393, 181e190. Norton, T.A., 1992. Dispersal by macroalgae. British Phycological Journal 27 (3), 293e301. Olenin, S., Labanauskas, V., 1994. Mapping of the underwater biotopes and spawning grounds in the Lithuanian coastal zone. Zˇuvininkyst_e Lietuvoje, 70e76 (in Lithuanian). Olenin, S., Daunys, D., Leinikki, J., 2003. Biodiversity Study and Mapping of Marine Habitats in the Vicinity of the Buting_e Oil Terminal, Lithuanian Coastal Zone, Baltic Sea. Joint FinnisheLithuanian Project Report. Coastal Research and Planning Institute, Klaip_eda University, Klaip_eda, 30 pp. Orav-Kotta, H., Kotta, J., 2004. Food and habitat choice of the isopod Idothea baltica in the northeastern Baltic Sea. Hydrobiologia 514, 79e85. Orav, H., Kotta, J., Martin, G., 2004. Factors affecting the distribution of benthic invertebrates in the phytal zone of the north-eastern Baltic Sea. Proceedings of the Estonian Academy of Sciences Biology Ecology 49 (3), 253e269. Orlov, I., 1965. About opportunities of industrial use of Furcellaria storm discharges in the Baltic Sea. Fisheries researches in the Baltic Sea. Simposium N7. Zvaigzne, Riga, pp. 130e137 (in Russian). Osborne, P.D., 2005. Transport of gravel and cobble on a mixed-sediment inner bank shoreline of a large inlet, Grays Harbor, Washington. Marine Geology 224, 145e156. Padilla, D.K., 1993. Rip stop in marine algae: minimizing the consequences of herbivore damage. Evolutionary Ecology 7, 634e644. Quinn, G.P., Keough, M.J., 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, 520 pp. Ronnberg, O., Lax, P.F., 1980. Influence of wave action on morphology and epiphytic diatoms of Cladophora glomerata (L.) Kutz. Ophelia (Suppl. 1), 209e218. Ruuskanen, A., Back, S., 1999. Morphological variation of northern Baltic Sea Fucus vesiculosus L. Ophelia 50 (1), 43e59. Sanderson, J.C., 1957. Subtidal macroalgal assemblages in temperate Australian coastal waters, Australia: State of the Environment Technical Paper Series (Estuaries and the Sea). Department of the Environment, Canberra, 129 pp. Snoeijs, P., 1999. Marine and brackish waters. Acta Phytogeographica Suecica 84, 187e212. StatSoft Inc., 2006. Electronic Statistics Textbook. StatSoft, Tulsa, OK. Available from: . Thomsen, M.S., Wernberg, T., Kendrick, G.A., 2004. The effect of thallus size, life stage, aggregation, wave exposure and substratum conditions on the forces required to break or dislodge the small kelp Ecklonia radiata. Botanica Marina 47 (6), 454e460. Thomsen, S.M., Thomas, W., 2005. Miniview: what affects the forces required to break or dislodge macroalgae? European Journal of Phycology 40 (2), 139e148.

316

M. Bucas et al. / Estuarine, Coastal and Shelf Science 75 (2007) 308e316

Trei, T., 1984. Commercial phytobenthos species. In: Essays on the Baltic Sea biological productivity (Ocherki po biologicheskoj produktivnosti Baltijskogo morja, T.1). Moscow, pp. 354e364 (in Russian). Underwood, A.J., Chapman, M.G., 1998. Variation in algal assemblages on wave-exposed rocky shores in New South Wales. Marine and Freshwater Research 49, 241e254. Wallentinus, I., 1979. Environmental influences on benthic macrovegetation in the TrosaeAsko¨ area, Northern Baltic proper. II. The ecology of macroalgae and submerged phaneorgasm. Contributions from the Asko¨ Laboratory, University of Stockholm 25, 1e210. Wallentinus, I., 1991. The Baltic Sea gradient. In: Mathisen, A.C., Nienhuis, P.H., Goodall, D.W. (Eds.), Intertidal and Littoral Ecosystems. The Ecosystems of the World, vol. 24. Elsevier, Amsterdam, pp. 83e108. Wentworth, C.K., 1922. A scale of grade and class terms for clastic sediments. Journal of Geology 30, 377e392.

Worm, B., Lotze, H.K., Bostrom, C., Engkvist, R., Labanauskas, V., Sommer, U., 1999. Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Marine Ecology Progress Series 158, 309e314. Zˇaromskis, R., 1982. Storm effects upon the Lithuania coast. Annals of Geography 20, 93e100 (in Lithuanian). Zˇaromskis, R., 1992. Morphological peculiarities of coastal zone of the landscape in basins with different dynamic regime. In: Vaitekunas, S., Minkevicius, V. (Eds.), Geography in Lithuania. Geographical Society of Lithuania, Vilnius, pp. 44e68. Zˇaromskis, R., 1994. Dynamics and silt traffic of bottom surface. In: Lazauskas, J. (Ed.), Oil Terminal in Buting_e. Baltic ECO, Vilnius, pp. 54e70 (in Lithuanian). Zuur, A.F., Ieno, E.N., Smith, G.M., 2007. Analysing ecological data. Series: Statistics for Biology and Health. Springer, 700 p.