Effect of abiotic environment on the distribution of the attached and drifting red algae Furcellaria lumbricalis in the Estonian coastal sea/Punavetikas agariku (Furcellaria lumbricalis) kinnitunud ja triiviva vormi levikumustrit kujundavad abiootilised tegurid Eesti rannikumeres.
Furcellaria lumbricalis (Hudson) J. V. Lamouroux is an abundant member of the marine flora in colder waters of the North Atlantic and Arctic oceans. The species is one of the few rhodophytes that prevails in the brackish Baltic Sea (Novaczek & Breeman, 1990; Bird et al., 1991; Nielsen et al., 1995). Furcellaria lumbricalis is the only economically important red algal species in the Baltic Sea and has been exploited in the study area since the 1960s (Trei, 1978; Martin et al., 2006a). Besides its economic value, the loose-lying macroalgae enhance the diversity of macroinvertebrates by offering a secondary substrate for several true hard-bottom species (Kotta et al., 2000; Kotta & Orav, 2001; Orav-Kotta & Kotta, 2004; Lauringson & Kotta, 2006).
There exist attached and drifting forms of F. lumbricalis. Bird et al. (1991) give an adequate review on the morphological differences between these distinct forms. Furcellaria lumbricalis can be confused with Polyides rotundus (Hudson) Gaillon, but F. lumbricalis lacks discoid holdfast and has wider branching angles compared to P. rotundus (Waern, 1952; Dixon & Irvine, 1977; Guiry & Guiry, 2009). The attached form of F. lumbricalis can be found practically throughout the photic range on hard substrates at salinities down to 4 (Snoeijs, 1999; Martin, 2000; Kotta & Orae, 2001; Kostamo, 2008). The attached F. lumbricalis has sexual and sporangial reproduction (Austin, 1960a, 1960b). In particular, sexual reproduction occurs occasionally and clonality is a common phenomenon in the northern Baltic Sea (Kostamo, 2008). Besides the attached form the West Estonian Archipelago Sea hosts a drifting red macroalgal community dominated by F. lumbricalis (= forma aegagropila) and the drifting form of Coccotylus truncates (Pall.) M. J. Wynne & J. M. Heine. The community is truly unique in European seas and is likely maintained by the prevailing circular currents and the grid of islets that surround the area (Martin, 2000). Unlike the common attached F. lumbricalis, the drifting (also known as loose-lying, unattached, free-living, free-floating) form of the species appears only in sterility and reproduces only vegetatively, mainly by fragmentation (Austin, 1960c; Norton & Mathieson, 1983; Bird et al., 1991).
It is plausible that different environmental factors determine the patterns of attached and drifting forms of F. lumbricalis. In general, the large-scale distribution of F. lumbricalis is determined mainly by temperature. Within the optimum temperature range the species inhabits lower intertidal and subtidal hard bottoms and tolerates reduced salinities (Luning, 1990; Guiry & Guiry, 2009). Within the Baltic Sea salinity is likely the most important factor setting the regional distribution limits of algal species (Kautsky & Kautsky, 2000) and within the optimum salinity range substrate type is considered to be the most important factor regulating local macroalgal community structure, including F. lumbricalis (Eriksson & Bergstrum, 2005). Earlier studies on the Baltic Sea red algal communities have shown that the type of substrate, wave exposure, and depth mainly explain the observed distribution patterns of the attached F. lumbricalis (Reitalu et al., 2002; Martin & Torn, 2004; Becas et al., 2007). However, the importance of different environmental factors that govern the distribution of macroalgal communities may vary among water basins (Martin, 2000).
Nowadays, the drifting F. lumbricalis can be found only in semi-exposed habitats in the Baltic Sea (Martin et al., 2006b) but it may also occur in the lochs of Scottish and Irish seas (Leering et al., 1969: 421). The drifting F. lumbricalis was previously found in Polish waters but the community disappeared due to elevated eutrophication in the 1980s (Kruk-Dowgiallo & Szaniawska, 2008). Intensive harvesting decimated the stocks of the drifting Furcellaria stocks in the central Kattegat in the 1950s-1970s (Lend & Christensen, 1969; Pedersen & Snoeijs, 2001). Our knowledge about abiotic factors affecting the spatial distribution of the drifting F. lumbricalis is scanty but it is likely that the observed patterns are due to impoverished light conditions (Martin et al., 2006b). Besides, as most of the unattached algae, the drifting F. lumbricalis can grow in calm-water localities, where water motion is moderate avoiding seaweeds to wash ashore (Kain & Norton, 1990).
The aim of this study is to describe the biomass distribution patterns of attached and drifting forms of F. lumbricalis in the whole Estonian
coastal sea including the Gulf of Riga, the West Estonian Archipelago Sea, the Gulf of Finland, and the Baltic Proper. We also seek which environmental variables best predict the observed biotic patterns as such analyses enable us to reveal the causality of interactions between abiotic environmental variables and macrophyte species.
Earlier studies on F. lumbricalis have covered small areas, i.e. had a small range of environmental variability (Plinski & Florczyk, 1984; Makinen et al., 1988; Bergstrdm & Bergstrdm, 1999; Martin & Torn, 2004; Eriksson & Bergstrdm, 2005; Bucas et al., 2007). Besides, many of these studies used algal cover as a proxy of density estimate. In field, however, the cover of F. lumbricalis is often 100% and in such habitats the direct estimate of biomass (in g dw m 2) would be a much more useful indicator of algal spatial patterns. There is only one investigation (Reitalu et al., 2002) that covers the large-scale distribution of macroalgal communities along the Estonian coasts, but this study had a small number of samples, did not involve semi-enclosed marine habitats, and mostly emphasized classification of seaweed associations. On the larger spatial scales we are also aware but of three large-scale mapping studies of macrophyte communities in the Baltic Sea area (Kautsky & Kautsky, 1989; Middelboe et al., 1997; Snoeijs, 1999). However, the results of these studies were based on communities inhabiting the coastal sea of Scandinavia and did not cover the broad range of the mixed sediment types and wave exposure conditions that can be observed in the Estonian coastal range. To date we are not aware of any comparative studies where the distribution of different forms of F. lumbricalis is analysed in a systematic and comprehensive framework.
MATERIAL AND METHODS
This study was carried out in the eastern Baltic Proper, the Gulf of Riga, the West Estonian Archipelago Sea, and the Gulf of Finland. The Baltic Proper is the largest subdivision of the Baltic Sea with nearly 211 000 [km.sup.2] surface area. The average sea surface temperature in winter is around 2[degrees]C and annual surface layer salinity is 6-7 (Schramm, 1996). During August, the mean sea surface temperature is 15-16[degrees]C in the northern part of the Baltic Proper (Falandysz et al., 2000). Due to the absence of freshwater inflows the eastern Baltic Proper has the highest salinity in the Estonian coastal range. The dominating substrates are limestone rock, stones, sand, and a mixture of the above (Reitalu et al., 2002). The coasts of the eastern Baltic Proper are very exposed, hydrodynamically active, and in general characterized by a steep coastline (Suursaar et al., 2008). The phytobenthic communities in the eastern Baltic Proper are very diverse and penetrate deeper compared to the other studied water basins (Trei, 1987; Kautsky & Kautsky, 2000).
The Gulf of Riga is a wide, shallow, semi-enclosed brackish-water ecosystem of the Baltic Sea. A huge drainage area (134 000 [km.sup.2]) supplies the gulf with fresh water, which mostly enters the southern part of the basin. The average salinity varies from 0.5-2.0 in surface layers in its southern and northeastern areas to 7 in the straits. In most parts, however, the salinity is 5.0.5 and there is no permanent halocline. Due to the shallowness of the gulf, the dynamics of both its surface and deep water temperatures is directly coupled with air temperatures. In a 'typical' year the water is cold and no clear thermocline occurs until May. Later the surface water temperature rises to about 17-20[degrees]C, and a thermocline builds up. The thermocline reaches a depth of 25 m in August and disintegrates in September-October due to intensive wind mixing. In the course of autumn storms the surface water cools down and the deep water temperature rises to 5-10[degrees]C. The oxygen regime is relatively good due to strong vertical mixing. The gulf is on average twice as eutrophicated as the Baltic Proper, and the outflow of nutrients through the straits is higher than their inflow. In general, the bottom relief of the area is quite flat, with gentle slopes towards deeps. The northern part of the gulf is characterized by a wide coastal zone with diverse bottom topography and extensive reaches of boulders. The southern part of the Gulf of Riga is more exposed; steep and soft substrate prevails (Kotta et al., 2008a and references therein).
The West Estonian Archipelago Sea is the smallest studied basin with a surface area of 2243 [km.sup.2] (Suursaar et al., 2002). Salinity in this shallow area varies between 6 and 7. Temperature conditions resemble those of the Gulf of Riga. The region is periodically influenced by the nutrient-rich water of the Gulf of Riga. The state of the Gulf of Riga plays a significant role in the development of benthic communities in the West Estonian Archipelago Sea. The bottom relief of the area is flat, with gentle slopes towards deeps. The whole water basin is semi-exposed. Sand and sandy clay substrates prevail in the study area. Due to shallowness and clayey sediments already moderate winds result in strong resuspension of bottom sediments and poor underwater light conditions.
The surface area of the Gulf of Finland totals 30 000 [km.sup.2]. As compared to other basins in the Baltic Sea, the Gulf of Finland has a relatively large catchment area and the greatest freshwater inflow. Therefore the gulf has a strong horizontal salinity gradient. The surface salinity varies from 0 in its eastern end to 7 in the western areas (Pitkanen et al., 2008). Near the bottom, the salinity increases from 5 in the eastern parts to approximately 10 in the western parts. The strength of the halocline varies both spatially and temporally. The average seawater temperature varies from 0 to 15[degrees]C. The gulf is among the most eutrophicated basins in the Baltic Sea area (Pitkanen et al., 2007). Bottom sediments mainly consist of sand fractions and boulders at shallower areas and silt and clay sediments rich in organic matter in deeper areas (Pitkanen et al., 2008).
Sampling and sample analyses
The phytobenthos sampling and sample analysis followed the guidelines developed for the HELCOM COMBINE programme (HELCOM, 1999). The frame samples (400 [cm.sup.2] surface area) were collected randomly by a diver. A total of 386 stations were sampled and three replicate frame samples were taken in each station once a year in summers 2007 and 2008 (Fig. 1). Altogether 1158 phytobenthic samples were collected. During sampling the geographic coordinates, depth, and the coverage of different sediment types and phytobenthos were recorded. Average salinity values were obtained from the database of the Estonian Marine Institute.
Samples were preserved in a deep freezer at -20[degrees]C. In the laboratory, plants were counted and identified under stereo dissecting microscope. Dry weights of all taxa were obtained after keeping the material 2 weeks at 60[degrees]C. Prior to biomass measuring, all macroscopic epibionts were removed from F. lumbricalis thalli.
A simplified Wave Model method was used to calculate the wave exposure for mean wind conditions represented by the ten-year period between 1 January 1997 and 31 December 2006 (Isaeus, 2004). A nested-grids technique was used to ensure long distance effects on the local wave exposure regime and the resulting grids had a resolution of 25 m. The means and variability of the wave exposure were calculated at 25, 500, 1000, and 5000 m resolutions using the Spatial Analyst tool of ArcInfo software (ESRI, 2001).
The Spatial Analyst tool of ArcInfo software was also used to calculate the means and variability of the inclination of coastal slopes at 25, 500, 1000, and 5000 m resolutions based on depth charts (available at the Estonian Marine Institute). Coastal slope refers to the amount of inclination of sea bottom. Zero indicates flat bottoms and larger numbers indicate higher degrees of grade (i.e. depressions or hills). Resolution indicates the scale in which topographic features occur.
[FIGURE 1 OMITTED]
Multivariate data analyses were performed by the statistical program 'PRIMER' version 6.1.5 (Clarke & Gorley, 2006). Similarities between all pairs of samples were calculated using a zero-adjusted Bray-Curtis coefficient. The coefficient is known to outperform most other similarity measures and enables samples containing no organisms at all to be included (Clarke et al., 2006). BEST analysis (BIOENV procedure) was used to relate the patterns of environmental variables measured at a sampling unit. The analysis shows which environmental variables best predict the observed biotic patterns. A global BEST match permutation test was run to examine the statistical significance of the observed relationships between environmental variables and biotic patterns.
In this study altogether 360 samples of 1158 (i.e. 31%)consisting either of attached or drifting forms of F. lumbricalis were investigated. The attached form occurred in 23% of the samples and the drifting form in 8% of the samples taken within the Estonian coastal range in 2007 2008. Table 1 lists all studied abiotic environmental variables and shows the distribution of the attached and drifting F. lumbricalis along these environmental gradients (means and variability). Compared to the drifting form, the attached F. lumbricalis tolerated a broader range of environmental variability and reached down to the lowest benthic macrovegetation limits ever monitored in the Estonian coastal sea (i.e. 18 m in the offshore waters of NW Hiiumaa Island, according to the database of the Estonian Marine Institute). The drifting F. lumbricalis occurred on average deeper than the attached F. lumbricalis but its depth range was smaller, estimated at 1-8.5 m. On the other hand, the biomass of the drifting form varied in a wider range than the attached F. lumbricalis.
The biomasses of both drifting and attached forms of F. lumbricalis reached up to 500 g dw [m.sup.-2]. The attached F. lumbricalis was found all around the Estonian coastal waters except for the eastern Gulf of Finland, where the species was limited by the 4.8 psu isoline (compare Fig. 1 and Fig. 2), the central West Estonian Archipelago Sea, and the offshore waters of NW Hiiumaa Island. The biomasses were relatively large in the open Baltic Proper, especially adjacent to Saaremaa Island. The biomasses were relatively moderate and variable in the Gulf of Finland and the Gulf of Riga (Fig. 2). The drifting form of F. lumbricalis was found only in the West Estonian Archipelago Sea, except of one site at the northern coast of the Gulf of Riga (Fig. 3).
The BEST permutation test showed that the biomass distribution of the attached F. lumbricalis was best predicted by the combination of wave exposure, depth, and the percentage of gravel and pebble fractions at local scale (Rho 0.178; p < 0.001). Within the studied range increasing depth and wave exposure resulted in higher biomasses of the attached F. lumbricalis. On the other hand, the increasing percentage of gravel and pebble fractions in the sediment reduced the biomass of the attached F. lumbricalis. Surprisingly, salinity had no significant effect on the distribution and biomass of the attached F. lumbricalis along the Estonian coastal sea.
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
The biomass distribution of the drifting F. lumbricalis was best explained by the combination of wave exposure and bottom slope at 500 m scale. However, this interaction was significant only if there was no hard substrate available (Rho 0.378; p < 0.001). On soft bottoms the biomass of the drifting F. lumbricalis decreased with increasing slope and variability of wave exposure at the respective scale. On hard bottoms within the studied range of exposure and slope the community consisted of the attached F. lumbricalis.
The study showed that (1) the combination of multiple environmental variables explained the distribution of attached and drifting forms of F. lumbricalis and (2) different environmental variables were important for different forms of the red alga. Increased affinity of F. lumbricalis to deeper areas refers to the ability of the species to tolerate poorer light conditions compared to other macroalgae inhabiting the Estonian coastal sea (Paalme & Kukk, 2003).
Lowered preference of the attached F. lumbricalis to the bottoms dominated by gravel and pebbles is related to sediment instability as in such sediments F. lumbricalis can be dislodged during storms (Thomsen & Wernberg, 2005; Bucas et al., 2007). Increased affinity of the attached F. lumbricalis to elevated wave exposure suggests that the species prefers habitats where the competitive interactions among the macroalgae are the weakest (Kiirikki, 1996; Eriksson & Bergstrdm, 2005) as highly exposed areas are characterized by low biomasses of perennial macrovegetation (Pratt & Johnson, 2002; Reitalu et al., 2002). However, too high wave exposure levels render habitat inhospitable for the attached F. lumbricalis (Bucas et al., 2007) but such values do not occur in the northeastern Baltic Sea. As such, the results agree with previous observations in the northern areas of the Gulf of Finland where a positive correlation between wave exposure and the biomass of F. lumbricalis was reported (Westerbom et al., 2008).
Surprisingly, salinity had no significant effect on the distribution and biomass of the attached F. lumbricalis along the Estonian coastal sea. Similarly, Kornfeldt (1979) reported no effect of salinity on the biomass of this algal species. The lack of a clear-cut effect suggests that the growth of the red alga is not affected by shifts in salinity at the lower limit of its salinity tolerance.
Strong links between wave exposure, bottom slope at 500 m scale, and the distribution of the drifting F. lumbricalis suggest that the mesoscale seabed topography and hydrodynamic regime largely determine the distribution pattern of this red algal form. Weak depressions of 500 m spatial scale and uniform wave regime seem very important for drifting algal mats to remain in the study area. However, this interaction was significant only if there was no hard substrate available. On hard bottoms within the studied range of exposure and slope the community consisted of the attached F. lumbricalis.
This implies that interspecific interactions between the attached and drifting forms of F. lumbricalis are behind the observed distribution pattern of the drifting F. lumbricalis. Both the attached and drifting F. lumbricalis tolerate poor light conditions. However, the growth rates of different forms vary depending on the depth (light conditions) considered. On shallower areas the growth rate of the attached F. lumbricalis is higher than that of the drifting form and therefore the attached F. lumbricalis may outcompete the drifting form in such habitats (Martin et al., 2006b). In deeper areas (i.e. at poorer light conditions), however, the drifting form has an advantage over the attached form in terms of the growth rate. Similarly, the habitats that have a large share of clay and sand fractions are characterized by high sediment resuspension, sedimentation rates, low light levels, and thus are very inhospitable for the most of macroalgae (Kain & Norton, 1990; Eriksson & Johansson, 2005) but not so for the drifting F. lumbricalis (Martin et al., 2006b).
Moreover, the drifting F. lumbricalis hosts another red algal species Coccotylus truncates (Kersen & Martin, 2007). A recent experimental study demonstrated that the growth of the red algae in such an inhospitable environment is highly density dependent (Kotta et al., 2008b) and thus the biomass pattern of the drifting F. lumbricalis is likely determined by the share of C. truncates in the community. Total biomass values of the drifting F. lumbricalis and C. truncates are set by regional weather conditions that (mainly through wind patterns) determine the underwater light regime and also influence seawater temperatures that are known to affect the growth of F. lumbricalis (Bird et al., 1979; Rueness & Tananger, 1984). It is likely, however, that large-scale abiotic variables primarily determine the broad patterns of the studied red algal species and within these broad patterns the competitive interactions among macroalgae modify algal distributions.
To conclude, our study showed that the attached F. lumbricalis prefers deep and exposed sea areas with bottoms not containing mobile sediment fractions. In other words, the attached F. lumbricalis is confined to the areas where the growth of other macroalgal species is suppressed either due to poor light conditions or elevated wave exposure (instability of sediments) and thereby the competitive interactions among the macroalgae are the weakest. The drifting F. lumbricalis is confined to deep habitats that are characterized by a weak topographic depression, soft bottoms, high sediment load, and poor light conditions. Such habitats are unsuitable for the other macroalgae (except for the drifting form of C truncates) and the attached F. lumbricalis. Because of its loose-lying nature, the spatial patterns of the drifting F. lumbricalis are mainly determined by the basin-scale hydrodynamical (light) regime and partly by the competitive interactions among other species within the drifting macroalgal community. In order to reveal the exact mechanisms and interactions, however, experimental studies with manipulated wave exposure, light conditions, sediment loading, and algal biomasses are needed.
The work was supported by target-financed project SF0180013s08 of the Estonian Ministry of Education and Research and by the Estonian Science Foundation under grants 6016, 6750, and 7813.
Received 16 March 2009, revised 25 September 2009
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Priit Kersen (a, b) ([mail]), Helen Orav-Kotta (a), Jonne Kotta (a), and Henn Kukk (b)
(a) Estonian Marine Institute, University of Tartu, Maealuse 10a, 12618 Tallinn, Estonia
(b) Institute of Mathematics and Natural Sciences, Tallinn University, Narva mnt. 25, 10120 Tallinn, Estonia
([mail]) Corresponding author, firstname.lastname@example.org
Table 1. Main environmental characteristics associated to attached and drifting forms of F. lumbricalis in the Estonian coastal sea. Only the samples in which F. lumbricalis was present were used Variable Attached F. lumbricalis (n = 272) Range Mean [+ or -] SE (min to max) Biomass, g dw 0.015 ... 490.88 37.64 [+ or -] 0.03 [m.sup.-2] Depth distribution, 0.1 ... 17 5.45 [+ or -] 0.24 m Wave exposure, 13 106 ... 968 172 256 328 [+ or -] 15 598 [m.sup.2] [s.sup.-1] Coastal slope 25 m 0.00 ... 8.46 0.48 [+ or -] 0.07 scale, [degrees] Coastal slope 500 m 0.00 ... 2.65 0.19 [+ or -] 0.02 scale, [degrees] Coastal slope 1000 0.00 ... 1.40 0.19 [+ or -] 0.02 m scale, [degrees] Coastal slope 5000 0.00 ... 0.38 0.08 [+ or -] 0.01 m scale, [degrees] Salinity 4.78 ... 6.55 5.76 [+ or -] 0.03 Sediment type, % of bottom coverage Clay 0 ... 50 0.55 [+ or -] 0.26 Silt 0 ... 100 3.02 [+ or -] 0.88 Sand 0 ... 100 27.27 [+ or -] 2.06 Gravel + pebbles 0 ... 98 6.35 [+ or -] 1.00 Shingle 0 ... 80 30.78 [+ or -] 2.01 Boulder 0 ... 100 14.31 [+ or -] 1.40 Rock 0 ... 100 12.41 [+ or -] 1.81 Variable Drifting F. lumbricalis (n = 88) Range Mean [+ or -] SE (min to max) Biomass, g dw 0.33 ... 568.58 210.02 [+ or -] 13.23 [m.sup.-2] Depth distribution, 1 ... 8.5 7.05 [+ or -] 0.13 m Wave exposure, 36 450 ... 145 517 85 397 [+ or -] 3 369 [m.sup.2] [s.sup.-1] Coastal slope 25 m 0.00 ... 1.29 0.11 [+ or -] 0.03 scale, [degrees] Coastal slope 500 m 0.00 ... 0.19 0.02 [+ or -] 0.003 scale, [degrees] Coastal slope 1000 0.002 ... 0.12 0.03 [+ or -] 0.004 m scale, [degrees] Coastal slope 5000 0.01 ... 0.04 0.02 [+ or -] 0.001 m scale, [degrees] Salinity 5.54 ... 5.83 5.76 [+ or -] 0.004 Sediment type, % of bottom coverage Clay 0 ... 75 18.47 [+ or -] 1.68 Silt 0 ... 30 0.74 [+ or -] 0.39 Sand 25 ... 100 79.83 [+ or -] 1.64 Gravel + pebbles Absent Absent Shingle 0 ... 10 0.57 [+ or -] 0.23 Boulder 0 ... 20 0.4 [+ or -] 0.26 Rock Absent Absent
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|Author:||Kersen, Priit; Orav-Kotta, Helen; Kotta, Jonne; Kukk, Henn|
|Publication:||Estonian Journal of Ecology|
|Date:||Dec 1, 2009|
|Next Article:||Important scales of distribution patterns of benthic species in the Gretagrund area, the central Gulf of Riga/Pohjaelustiku liikide...|