Hydrobiologia 459: 83–102, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
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Patterns of macroalgal diversity, community composition and long-term changes along the Swedish west coast M. Peders´en1 & P. Snoeijs2∗ 1 Department
of Botany, Stockholm University, SE-10691 Stockholm, Sweden of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavägen 14, SE-75236 Uppsala, Sweden Tel: +18-471-28-85. Fax: +18-553-419. E-mail:
[email protected] (∗ Author for correspondence) 2 Department
Received 15 November 2000; in revised form 21 May 2001; accepted 1 June 2001
Key words: algae, ecology, depth distributions, diversity, long-term changes, Kattegat, Skagerrak
Abstract This study analyses the complicated patterns of vertical distribution of the macroalgal vegetation in an area where brackish and marine waters meet and mix. Variables used to record vegetation characteristics are algal cover, species composition and diversity. The data set includes 64 diving profiles, all from sites exposed to wave action, along a ca. 260 km long coastline. The profiles belong to four categories: coastal sites in the Skagerrak (more marine), coastal sites in the Kattegat (more brackish), coastal sites in the Kattegat after a toxic phytoplankton bloom, and submerged offshore stone reefs in the Kattegat. The highest species diversity was found at the reefs, which are not affected directly by land runoff. At the reefs the 18 most common perennial species penetrate 2–11 m (on average 5.5 m) deeper than at the coastal sites. The virtual absence of sedimentation, and thus the availability of substratum, at the reefs may explain the differences so that the lower limit for the algae is determined by light penetration or by recruitment problems caused by strong currents at the reefs, whereas sedimentation limits the settlement of algae in coastal sites. Ordination analysis based on species composition reveals that the major environmental gradients structuring the algal vegetation in the Kattegat and the Skagerrak are salinity and water depth. The large data set of this study made it possible to quantify the downward dislocation of Atlantic intertidal species to the sublittoral along the Swedish west coast. For example, the mean upper limit of Corallina officinalis is 2 m in the Skagerrak but 12.5 m in the Kattegat and the mean occurrence interval of Fucus serratus is 0.9–2.7 m in the Skagerrak, but 1.1–6.3 m in the Kattegat. This downward dislocation is suggested to be the result of decreased competition when species successively disappear with lower salinity. Comparisons of the present study’s results with those of previous investigations show that eight common red algal species have moved upwards compared to the situation before the large-scale eutrophication started in the 1960s, e.g. Cystoclonium purpureum and Polysiphonia elongata by ca. 8 m, Phycodrys rubens and Delesseria sanguinea by ca. 5 m. A toxic phytoplankton bloom affected macroalgal community composition on the whole only slightly, but it had a negative effect on algal cover and species richness below a water depth of ca. 5 m, the algae were visibly damaged and the lower vegetation limit temporarily moved upwards.
Introduction This paper presents the results from a large-scale field study of the macroalgal vegetation in the Skagerrak and Kattegat in 1988–1990. The study was carried out to be able to compare the littoral vegetation with earlier records to understand the effects of large-scale
environmental changes in the ecosystem. It also documents the short-term effects of a toxic phytoplankton bloom that struck the area in spring 1988. Only waveexposed sites in open waters were included in the study because these will reflect large-scale changes and not local pollution. This study further makes comparisons between the more marine Skagerrak and the
84 more brackish Kattegat and includes the major submerged offshore stone reefs (‘fishing-banks’) in the Kattegat. The latter are previously little known hot spots of algal diversity in the area. Our study will also serve as a comprehensive baseline study for future investigations of the macroalgal vegetation of the area. Previous large-scale phycological studies in this area were predominantly floristically inclined (Kylin, 1907, 1944, 1947, 1949; Rosenvinge, 1909–1931; Rosenvinge & Lund, 1941–1947; Lund 1950). Wærn (1952, 1965) described ecological communities and processes in a wider perspective, but unfortunately also without a numerical basis for documenting these communities and processes, except for single welldescribed diving profiles, some of which recently have been re-investigated (e.g. Johansson et al., 1998). Further recent investigations were also restricted to single areas or localities, e.g. at Kullen in the southern Kattegat by von Wachenfeldt (1975) and Kornfeldt (1981, 1984), and at Lysekil in the Skagerrak by Lundälv et al. (1986) and Svane & Gröndahl (1988). Contrarily, our study covers a 260 km long coastline and thus the major part of the Skagerrak and Kattegat. In the early days, algal collections were mainly made by dredging (instead of diving), and such data must be interpreted with caution because of interfering loose-lying algae and other anomalies, see the discussions in Michanek (1967), Nielsen (1991) and Nielsen & Dahl (1992a, b). Thus, no reliable data are available for direct comparative numerical vegetation analyses for the Kattegat and Skagerrak area as a whole to compare the situation before and after the extensive eutrophication that started in the 1960s (Rosenberg et al., 1990; Richardsson & Heilman, 1995). However, in the present study, we were able to make comparisons for the depth distributions of a number of common species for which the occurrence (but not abundance) with respect to water depth was well described by Kylin in the 1940s. The Skagerrak and Kattegat together form the northern part of the transitional zone between the marine North Sea and the brackish Baltic Sea. The Baltic current (outflow from the Baltic Sea) flows at the surface and its vertical extension strongly depends on wind direction. A halocline separates this surface layer from the high-salinity North Sea water (32–34 psu) beneath it. In this highly dynamic area, it is impossible to relate the distribution of macroalgae, which have been growing for months or years, to measured environmental factors such as temperature, irradiance or salinity. Constantly differing weather conditions affect
flow directions and mixing processes. There are, however, well-defined differences in salinity between the two basins (Fonselius, 1995): surface-water salinities are 15–25 psu in the Kattegat and 20–30 psu in the Skagerrak, the halocline is found at 20–30 m depth in the southern Kattegat and at 10–20 m in the eastern Skagerrak. There are probably also differences in sedimentation load between coastal sites (directly affected by land-runoff) and offshore submerged stone reefs (not affected by direct land-runoff), simply because of their geographical position. Minuscule tidal fluctuation (less than ca. 20 cm) is a typical feature at the rocky shores of the Swedish west coast and water level is mainly regulated by atmospheric pressure (Fonselius, 1995). This, together with the salinity gradient, creates special conditions that greatly affect the structure and composition of the algal vegetation. The typical Atlantic intertidal belt becomes lost with the reduction and final disappearance of tidal movements along a gradient from the northeastern Skagerrak to the southern Kattegat. Simultaneously, the water becomes increasingly brackish along this gradient. Many marine rocky-shore macroalgae that on the Atlantic and North Sea coasts are found in intertidal and upper littoral zones occur at increasingly greater water depth when following the salinity gradient from the Skagerrak through the Kattegat, the Öresund and finally into the Baltic Sea. This phenomenon has been defined as the ‘downward process’ (Wærn, 1952; 1965). It has been explained by the absence of tides, avoidance of more variable surface salinities and changes in competitive balance when marine species successively disappear along the salinity gradient and euryhaline species (the intertidal species from the Atlantic coast) compete for sublittoral space. The downward process is especially conspicuous for the large canopy- and belt-forming brown algae such as Fucus and Laminaria species (Wærn, 1965; Snoeijs, 1999). An example of a species that expands its depth range tremendously is Fucus vesiculosus, which is the only large perennial canopyforming alga that penetrates into the brackish waters of the Baltic Sea as far as the Gulf of Bothnia. On the Swedish west coast it has a depth range of ca. 20 cm only, but in the northern Baltic Sea proper it forms belts between a depth of 1 and 10 m in the absence of competitors. To be able to resolve the downward process, one has to disregard subordinate gradients such as differences in exposure, aspects of inner and outer archipelagos, bottom configurations and substrata and the orientation of the rocks in relation to the light
85 (Wærn, 1965). In the present study, it was for the first time possible to quantify the downward process from the Skagerrak to the Kattegat for the species that are common in both areas, because of the large quantity of data we collected from exposed sites. A larger number of previous studies has described changes in the macroalgal vegetation as a result of eutrophication or decreased eutrophication of bays and fjords of the Kattegat and Skagerrak (e.g. Klavestad, 1978; Wennberg, 1987; Bokn et al., 1992; Wallentinus, 1996). A common phenomenon of the decline or deterioration of algal communities in bays and fjords caused by eutrophication or other human impacts such as direct effects of municipal discharges (Norin & Wærn, 1973), ferry traffic (Rönnberg, 1981), pulp-mill effluents (Kautsky et al., 1988), cooling water discharge (Snoeijs & Prentice, 1989; Snoeijs, 1992), fish farming (Rönnberg et al., 1992), etc. is the loss of functional diversity. This does not necessarily include lower species diversity, because all large leaf-like canopy-forming perennial algae can be lost whereas the group small filamentous ephemeral algae becomes richer in species (Snoeijs & Prentice, 1989). Such a loss of important functional algal groups may affect a whole ecosystem because many invertebrates and fish are, at least part of their lives, dependent on the perennial algal belts for substratum, food and shelter. An example of this is the decline and the decreased depth penetration of the Fucus vesiculosus belt all around the Baltic Sea coasts (Kangas et al., 1982; Kautsky et al., 1986; Vogt & Schramm, 1991; Schramm, 1996; Eriksson et al., 1998). Therefore, we have tried in this paper to summarise different aspects of the algal vegetation in terms of functional diversity at exposed sites, thus reflecting the situation in the open waters. The phylogenetic groups (red, brown and green algae) summarise much of the physiological performances of the species. Algal functional types can roughly be summarised by size and shape classifications. Littler & Littler (1980) and Littler et al. (1983) found that thin, rapidly growing, short-lived algae are characteristic for unstable environments, whereas coarse, slower-growing, long-lived algae are characteristic of stable (late-successional) environments. Functional diversity is here derived by a deductive approach classifying the different algal species into groups of functionally similar species (types) which are expected to be critical in determining the operation (function) of the submerged littoral vegetation. In modelling terrestrial plant communities, functional types are seen as a necessary device for
reducing the complexity and often uncharted characteristics of species diversity in function and structure (Woodward & Cramer, 1996). One of the aims of this study was to test if such an approach can be useful for an algal vegetation. In this paper we report on the depth distributions of both species diversity and functional diversity of the vegetation according to salinity (Kattegat compared with Skagerrak), sedimentation (coastal sites compared with offshore submerged stone reefs in the Kattegat), and the occurrence of a shortterm catastrophe (a toxic pelagic microalgal bloom in the Kattegat). Materials and methods Fieldwork The rocky-shore macroalgal vegetation in the Swedish part of the Kattegat and the Skagerrak was investigated by SCUBA diving during four expeditions, 3–29 September 1988, 4–24 June 1989, 3–14 September 1989 and 7–27 June 1990, with the Uppsala-based research vessel ‘MS Sunbeam’. Two winter dives from land in February 1990 were included as well. Altogether ca. 150 forty-five – sixty min dives were performed within this project with 4–6 divers participating in each. In every dive, at least two divers were PhD-students in phycology or professional phycologists (one for video-filming and one for making notes and sampling of algae), and the others were assistants for photographing and carrying sampling bags. At each diving profile (5–10 m wide) the abundance of each encountered upright (non-crustose) species was recorded for every metre depth interval between the upper and lower occurrence of the algal vegetation, except for the upper metre of the littoral, which was subdivided into 0–0.5 and 0.5–1 m depth intervals. For the estimation of species abundance, a 0–5 ordinal scale was used which is suitable for underwater conditions when only limited time is available for recording the vegetation: 0: not found, 1: one individual, 2: several individuals, 3: common, 4: abundant, 5: dominant). The recording of the vegetation was achieved by (1) underwater notes on paper for each depth interval, (2) spoken records during video-filming for each depth interval, (3) sampling of algae for each depth interval, (4) photographic records. Special attention was given to detecting the lowest horizontal depth occurrences of macroalgae in the lower littoral. The criteria we used for determining the lowest limit of an alga are those of professor Mats Wærn
86 (pers. comm.): the alga has to grow attached to a horizontal substratum so that it will receive the maximum possible light dose, there must be possibilities to settle further down as well and algae growing on small stones or loose shells should not be considered because these may have fallen down from more shallow depths or may have been transported by currents. Identification of the algal samples, if necessary using light microscopy, and ‘ecological’ herbarium sheets on which all species from a certain depth are gathered on the same sheet were made by a crew of scientists and their assistants on board of ‘MS Sunbeam’. The scientists had followed the underwater work on a TV-monitor and they had been able to instruct the divers via a telephone on board. With the help of the algal samples brought up, the divers notes were completed with rare and/or smaller species that were missing from the direct underwater observations. The video-films, photographic slides and herbarium sheets are kept at the Universities of Stockholm and Uppsala under the name ‘WWF 1988–1990’ and are meant to serve as a basis of reference for this and future studies. Data compilation In 1999 all herbarium sheets, video-films and photographic slides were re-investigated and doublechecked against the field notes. The algal cover, expressed as percentage of bottom surface covered by a three-dimensional macroalgal vegetation, was estimated from the video-films for each one-metre depth interval. Dubious profiles, e.g. when the divers were disturbed by technical problems, were deleted. Finally, 64 diving profiles from 38 wave-exposed sites along a ca. 260 km long coastline were selected for use in this paper (Fig. 1, Table 1). Fourteen of the sites were visited more than once, but the diving profiles were not situated in the same position on the different occasions. The data set with the 64 diving profiles was subdivided into four subsets of data: coastal sites in the Skagerrak 1989/1990 (SKAG; n=15), coastal sites in the Kattegat 1989/1990 (KAT; n=25), coastal sites in the Kattegat 1988 (KAT88; n=12) and submerged offshore stone reefs in the Kattegat 1989/1990 (KATREEF; n=12). In May–June 1988, a toxic bloom of the pelagic prymnesiophyte Chrysochromulina polylepis caused a major catastrophe in the surface waters of the Swedish west coast (Kaas et al., 1991; Maestrini & Granéli, 1991). Most anim-
Figure 1. Map of the Swedish west coast, showing the locations of the diving sites 1–38 cf. Table 1.
als above the halocline died, annual algae disappeared temporarily and perennial algae lost their annual parts. This still affected the macroalgal vegetation in the open Kattegat and Skagerrak in September 1988 and in the present study the effects of the bloom were investigated by comparing the vegetation in 1988 (KAT88) with that in 1989/1990 (KAT). The effects of sedimentation were studied by comparisons between coastal sites (KAT: directly affected by land-runoff) and offshore submerged stone reefs (KATREEF: not affected by direct land-runoff). The effects of salinity were studied by comparisons between coastal sites in the Skagerrak (SKAG: 20–30 psu) and coastal sites in the Kattegat (KAT: 15–25 psu). To be able to identify large-scale changes in the ecosystem, the depth distributions of 28 common algal species (our data) were used to make comparisons with previously published depth distributions of these species. As reference material we used Kylin (1944,
8 12 13 14 17 18
Kattegat stone reefs 1989, 1990
Skagerrak coastal sites 25 1989, 1990 26 27 28 29 30 31 32 33 34 35 36 37 38
1 2 3 4 5 6 7 9 10 11 15 16 19 20 21 22 23 24
Kattegat coastal sites 1988, 1989, 1990
Marstrandsön Klädesholmen Skapholmen Bonden Skällholmen NW Skällholmen S Smedjebrottet Harpöbådar Flatholmen Sörgrundsberget Hållö Brimskär Ärholmen, Väderöarna Valön NW
NW of Hallands Väderö Stora Middelgrund Knölagrund Morups Bank Lilla Middelgrund Fladen
Ransvik Åkersberget Paradishamnen Visitgrottan Ablahamn Grytgrunden Svarteskär Hovs Hallar Påarpsrevet Tyludden Glommaryggen Glommens Fyr Äspevik Östra Sandan Arvaskär Lilleland Ölmeudde Kyrkefjällsund
Site nr Site name
Area
N, 12◦ 28 27 N, 12◦ 42 43 N, 12◦ 32 38 N, 12◦ 42 24 N, 12◦ 52 45 N, 12◦ 44 29 N, 12◦ 19 47 N, 12◦ 21 02 N, 12◦ 11 04 N, 12◦ 09 23 N, 12◦ 05 06 N, 11◦ 55 44 N, 12◦ 00 53 N, 11◦ 56 29
N, 12◦ 34 10 N, 12◦ 03 30 N, 12◦ 29 11 N, 12◦ 13 28 N, 11◦ 51 03 N, 11◦ 46 48 N, 11◦ 33 38 N, 11◦ 32 35 N, 11◦ 32 07 N, 11◦ 19 06 N, 11◦ 22 54 N, 11◦ 23 00 N, 11◦ 22 00 N, 11◦ 22 05 N, 11◦ 24 45 N, 11◦ 11 01 N, 11◦ 12 43 N, 11◦ 12 35 N, 11◦ 04 43 N, 11◦ 14 28
56◦ 18 08 56◦ 20 46 56◦ 26 11 56◦ 28 14 56◦ 37 06 56◦ 38 28 56◦ 55 49 56◦ 55 51 57◦ 11 22 57◦ 12 56 57◦ 13 32 57◦ 18 23 57◦ 21 28 57◦ 22 17 56◦ 28 08 56◦ 32 54 56◦ 50 49 56◦ 52 36 56◦ 55 00 57◦ 08 48 57◦ 53 28 57◦ 56 41 57◦ 56 44 58◦ 12 35 58◦ 14 59 58◦ 14 54 58◦ 15 28 58◦ 15 42 58◦ 15 43 58◦ 17 20 58◦ 20 34 58◦ 21 02 58◦ 34 46 58◦ 35 20
56◦ 17 28 N, 12◦ 28 54 56◦ 17 53 N, 12◦ 27 08 56◦ 18 13 N, 12◦ 27 07 56◦ 18 13 N, 12◦ 27 57
Position
Table 1. Summary of diving sites, including dates and depths of investigation
E E E E E E E E E E E E E E
E E E E E E
E E E E E E E E E E E E E E E E E E
890617: 0–10 m 890618: 8–18 m 890618: 0–18 m 890620: 0–18 m 900621: 0–10 m 900621: 0–15 m 900627: 0–23 m 890619: 5–23 m, 900627: 5–24 m 890619: 0–7 m 900620: 10–27 m 890621: 8–22 m 900626: 0–17 m 890622: 0–24 m 890624: 0–17 m
890911: 10–18 m 890611: 8–9 and 11–12 m, 900610: 8–12 m 900613: 4–11 m 890612: 12–26 m, 890909: 13–26 m, 900611: 12–25 m 890908: 7–8 and 23–24 m, 900612: 9–10 m 890614: 9–11 m, 890903: 9–11, 12–13 and 19–20 m, 900618: 8–20 m
880903: 1–13 m, 900608: 1–15 m 890913: 0–21 m 890604: 7–21 m, 890912: 0-21 m, 900203: 0–20 m, 900607: 0–20 m 880904: 0–3, 8–9 and 12–13 m 880905: 0–18 m, 890605: 0-19 m, 890914: 0–18 m, 900202: 0–13 m, 900607: 0–20 m 900609: 1–10 m 880906: 0–11 m, 890608: 0–11 m 880908: 0–13 m, 890608: 0–12 m 880909: 6–9 m, 890610: 5–8 m, 890910: 8–10 m, 900614: 3–7 m 880910: 0–5 m, 890610: 0–6 m, 890905: 0–5 m, 900614: 0–5 m 880913: 5–7 m 880914: 0–5 m 880916: 0–5 m, 900616: 0–4 m 880918: 0–5 m, 890615: 0–5 m, 900616: 0–5 m 900617: 0–18 m 890615: 0.5–25 m 890618: 0–12 m 880921: 0–5 m
Date(s) and investigated depths
87
88 where our sites 1–5 also are situated. Therefore, his upper depth limits are valid for the southern Kattegat and his lower depth limits for the southern Öresund. Von Wachenfeldt’s investigations are based on both dredging and diving. The taxonomic nomenclature used throughout this paper is according to the official check-list of the Baltic Marine Biologists (Nielsen et al. 1995) Data analysis
Figure 2. Algal cover (a) and species richness (b) given as means per water depth interval for each of the subsets of data: coastal sites in the Kattegat 1989–1990 (KAT), coastal sites in the Kattegat 1988 (KAT88), offshore submerged stone reefs in the Kattegat 1989–1990 (KATREEF) and coastal sites in the Skagerrak 1989–1990 (SKAG). Error bars indicate standard error of the mean.
1947, 1949) who in these three books compiled his knowledge of the macroalgae of the Swedish west coast, which he gathered since he started his PhDstudies at Uppsala University in 1902 (PhD-thesis: Kylin, 1907). Kylin covered exactly the same area as we did, but unfortunately he rarely mentioned differences in depth distributions between the Kattegat and the Skagerrak (only for 7 of the 28 species). Therefore, his upper depth limits are valid for the northern Skagerrak and his lower depth limits for the southern Kattegat. Kylin’s investigations are based on dredging, and therefore, the lower limit is not completely trustworthy. The second study we used to compare our depth distributions with is von Wachenfeldt (1975). He made a detailed study of the vegetation in the Öresund in 1963–1972, the narrow sound between Sweden and Denmark south of our study area, including ‘Kullen’
Detrended Correspondence Analysis (DCA), implemented with the programme CANOCO 4 (ter Braak & þmilauer, 1998), was carried out to summarise overall patterns in the vegetation of the 64 diving profiles. Community diversity was calculated as species richness, Shannon index (log base=e) and, Pielou’s evenness measure (Diamond & Case, 1986). Further statistical tests, analysis of variance (ANOVA), unpaired t-test and Pearson’s product-moment correlation (Fowler et al., 1998), were performed with the MINITABTM statistical package. The categories for describing algal functional diversity were: (a) phylogenetic classification in red, brown and green algae, (b) classification into size groups of the maximum possible size for each species: 50 cm, and (c) classification into shape groups simplified after Littler & Littler (1980): filamentous (filaments 1 mm wide in at least part of the thallus) and leaf-like (most of the thallus flat). In the calculations all depths down to 27 m were included. If the lower limit of algal occurrence was set by sedimentation (reported by the divers), the cover and species richness from this limit down to 27 m were 0.
Results Algal cover The relationship between algal cover and water depth is shown in Figure 2a for each of the subsets of data. Correlation analyses showed significant negative associations between water depth and mean algal cover for SKAG (r=−0.86, p
