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A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae
Estuarine, Coastal and Shelf Science 73 (2007) 249e258 www.elsevier.com/locate/ecss
A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae Sonja Ra˚berg*, Lena Kautsky Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden Received 19 September 2006; accepted 12 January 2007 Available online 7 March 2007
Abstract Anthropogenic activities worldwide have contributed to vegetation changes in many coastal areas, changes that may in turn affect faunal and algal assemblages in the involved ecosystems. In the northernmost part of the Baltic Sea the salinity is extremely low (3e4) and the only structurally complex alga present is Fucus radicans. Since in this area F. radicans is living at its salinity tolerance limit, it is potentially very sensitive to environmental changes. Any change in salinity could thus alter the overall algal community, changing it to one dominated solely by filamentous algae. To determine the importance of F. radicans to the associated faunal community, we examined differences between the 2 main vegetation types present, i.e., F. radicans and filamentous algae, in the Krono¨ren marine reserve in the northernmost part of the Baltic Sea. A similar study was conducted in the Asko¨ area in the northern Baltic Proper, where the more-investigated Fucus vesiculosus is the only large fucoid present. The biomass of associated fauna was significantly higher in both the F. radicans and F. vesiculosus than in the filamentous algal vegetation at some, but not all, sites. The F. radicans community also displayed a greater diversity of associated fauna in 3 of 5 investigated Krono¨ren sites, whereas no difference in diversity was detected between F. vesiculosus and the filamentous algal vegetations in the Asko¨ sites. Furthermore, the F. radicans community displayed a different faunal community, being the only investigated algal community with a faunal community dominated by K-strategy species, according to abundanceebiomass comparison curves. This pattern may be due to the low epiphytic load on these Fucus plants. In contrast, the F. vesiculosus community, as well as the algal communities with no Fucus in both areas, had high biomasses of filamentous algae and an invertebrate fauna dominated by Chironomidae, occurring in great abundance but only with a low biomass. ANOSIM analyses of faunal composition demonstrated a significant difference between the 2 vegetation types in both areas, largely due to greater abundance of Gammarus spp. and Theodoxus fluviatilis in the fucoid vegetation. Differences observed between the F. radicans and filamentous algal vegetation types were generally more pronounced than those between F. vesiculosus and nearby filamentous algal vegetation. These observations may be due to abiotic factors that differ between the 2 investigated areas, factors such as depth distribution, wave action and eutrophication level. This study has demonstrated that the less-investigated F. radicans may be as important as the larger F. vesiculosus for the associated faunal assemblages. At the same time, the limited extent of F. radicans at shallower depths makes F. radicans vegetation potentially more vulnerable to anthropogenic changes, as declines in fucoid vegetation are usually first manifested in populations at their lower depth limits, whereas shallow populations are less affected. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Fucus radicans; Fucus vesiculosus; biodiversity; species composition; Baltic Sea; Baltic Proper; Bothnian Sea
1. Introduction Human activities are believed to have had major impacts on vegetation composition in coastal areas. For example, human * Corresponding author. E-mail address: [email protected] (S. Ra˚berg). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.01.005
trampling on rocky shores in the Mediterranean has decreased both algal cover and the canopy of dominant macroalgal species (Milazzo et al., 2002). Furthermore, seagrass communities in the tropics have been shown to have been indirectly affected by anthropogenic activities such as rapid deforestation, which increases the siltation of coastal ecosystems (Terrados et al., 1998). Moreover, pollution together with the outbreak of
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‘‘wasting disease’’ has been responsible for a large decline in eelgrass populations (den Hartog and Polderman, 1975). Changes in the abundance and/or composition of macrophytes, such as those listed above, may in turn affect other organisms in an ecosystem by altering associated invertebrate communities (Benedetti-Cecchi et al., 2001; Reed and Hovel, 2006; Wikstro¨m and Kautsky, 2006) as well as fish assemblages (Pihl et al., 1994; Guidetti et al., 2003). Shifts from macroalgal to filamentous algal species are also believed not only to reduce the availability of resources, such as food and shelter, for small faunal species such as crustaceans, but also to have additional negative effects on food webs by, for example, altering nutrient storage and reducing the nursery areas and prey of fishes (Kangas et al., 1982; Kautsky et al., 1992). The newly described canopy-forming alga Fucus radicans sp. nov. (Bergstro¨m et al., 2005) is the dominant, large, structurally complex brown alga that tolerates the low salinity (3e4) in the northern Bothnian Sea (Baltic Sea). Fucus radicans differs morphologically from the common fucoid species Fucus vesiculosus by having no bladders, narrower fronds, a bushier appearance and being smaller in size (Bergstro¨m et al., 2005). The populations of F. radicans in the northern Bothnian Sea exist at their lower salinity range limit and are thus vulnerable to any further reduction in salinity. The increasing probability of abrupt climate change due to anthropogenic activities (Alley et al., 2003), therefore, threatens F. radicans, since rising air temperatures may enhance freshwater run-off and further lower Baltic Sea salinity (Omstedt and Hansson, 2006). The fact that F. radicans populations are largely (ca. 80%) clonal and hence, have low genetic variation (Bergstro¨m et al., 2005; Tatarenkov et al., 2005) further reduces its ability to cope with reduced salinity. Cover of opportunistic algal species is on the contrary positively correlated with decreasing salinity (Krause-Jensen et al., 2007). Despite numerous studies documenting the importance of structuring macrophytes for the diversity of associated fauna, no studies of which we are aware have investigated the significance of F. radicans for the faunal community inhabiting the algal belt. In contrast to Fucus radicans, the closely related species Fucus vesiculosus, which also inhabits the Baltic Sea, has declined in many areas since the 1970s (e.g., Kautsky et al., 1986; Vogt and Schramm, 1991; Eriksson et al., 1998; Kotta et al., 2000). Unlike the Bothnian Sea, the Baltic Proper is regarded as eutrophied (Ro¨nnberg and Bonsdorff, 2004), which in turn has resulted in the enhanced production of annual filamentous algae (e.g., Cederwall and Elmgren, 1990; Bonsdorff et al., 1997). The decline of F. vesiculosus and its replacement with filamentous algal species in this area (Leppa¨koski et al., 1999; Worm et al., 1999) may partly be due to an indirect effect of eutrophication, since high nitrogen levels favour the growth of these algae through their higher surface area:volume ratio (Pedersen, 1995). The ongoing decline in Fucus vesiculosus populations has prompted studies of the difference in biodiversity between the F. vesiculosus and the filamentous algal vegetation types that occupy similar habitats in the northern (Kraufvelin and Salovius, 2004) and southern (Wikstro¨m and Kautsky, 2006)
parts, respectively, of the Baltic Proper. These 2 studies, being somewhat different in approach, arrived at contradictory results. For example, greater faunal biomass was harboured by F. vesiculosus than by filamentous algal vegetation in the southern Baltic Proper (Wikstro¨m and Kautsky, 2006), while no such difference was detected in the northern Baltic Proper (Kraufvelin and Salovius, 2004). Furthermore, species richness was greater in the filamentous algal vegetation in the northern Baltic Proper than in the corresponding F. vesiculosus vegetation (Kraufvelin and Salovius, 2004), while no difference in species richness was detected between the vegetation types in the southern Baltic Proper (Wikstro¨m and Kautsky, 2006). The present study aims to investigate and compare the diversity, composition, abundance and biomass of the associated macrofauna (‘‘fauna’’) among stands of Fucus radicans and Fucus vesiculosus (‘‘Fucoids’’) versus among stands of corresponding filamentous algae (‘‘Non-fucoids’’). We hypothesized that the Fucoids would harbour a greater diversity, abundance and biomass of associated fauna m2. We also hypothesized that the faunal species composition would differ significantly between the 2 algal vegetation types in their respective regions. These potential differences are explored by using different multivariate analyses, one being k-dominance curves (Warwick, 1986) as an illustration of the abundance and biomass evenness among taxa. These curves are used to visually represent whether or not the faunal community is characterised by K- or r-selected taxa. Under ‘‘stable’’ conditions, K-selected taxa with the attributes of, for example, large body size and rather constant population size are the competitive dominants (Warwick, 1986). During pollution and/or habitat degradation, however, these taxa are less favoured and opportunistic r-selected species with, for example, small body size and highly variable population size are the numerical dominants (Warwick, 1986). Furthermore, we compared the biomasses of the filamentous algae m2 of both the Fucoid and Non-fucoid vegetation types, to control for the fact that, according to, for example, Hagerman (1966), faunal abundance is positively correlated with the amount of filamentous algae. 2. Materials and methods 2.1. Study sites The field studies were carried out in July 2003 at 5 sites in the Krono¨ren marine reserve, northern Bothnian Sea (63 260 N, 19 250 E), and 5 sites in the Asko¨ area, northern Baltic Proper (58 490 N, 19 390 E). The sampled sites were within 5 km of each other and varied in terms of wave exposure. Wave exposure at each site was calculated as thePmaximum local fetch P using the formula Lf ¼ ( ci cos gi)/( cos gi), where Lf is the maximum local fetch (wave exposure) and ci is the distance in kilometers to the nearest land (Ha˚kansson, 1981). The distance was measured in 15 directions with deviation angles ( gi) of 6, 12, 18, 24, 30, 36 and 42 from a central radius and in the direction of the transect. The exposure was corrected for depth according to the formula Ez ¼ E0 ez, where E0 is the degree of exposure at
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the surface and Ez the degree of exposure at a depth of z meters. The sites are referred to as K1eK5 in Krono¨ren and A1eA5 in Asko¨, 1 being the most sheltered site and 5 the most exposed. The Ez values for the sites varied between 0.04 and 0.15 and 0.60 and 3.90 in Krono¨ren and Asko¨, respectively. Samples were collected from hard substrates (rocks or large boulders). The salinity at sampling, measured using the Practical Salinity Scale, was 4.5 in Krono¨ren, but can vary between 3.5 and 5 (Kautsky, 1989). The salinity in the Asko¨ area varies between 5.8 and 7 (Wallentinus, 1978) but was approximately 6 at the time of sampling. The Krono¨ren marine reserve in northern Bothnian Sea will hereafter be referred to simply as ‘‘Krono¨ren’’, while the Asko¨ area in the northern Baltic Sea will be referred to as ‘‘Asko¨’’. 2.2. Data collection and treatment A 0.2 m2 frame with attached net bag (1 mm mesh size) was used to collect samples of a standardized size. Six replicates were randomly sampled in patches with and without fucoids at each site, in the upper parts of the fucoid belt where the fucoid cover was approximately 60% with small variations between sites and areas. In Krono¨ren, samples were taken at a depth of approximately 4 m and in Asko¨ at 0.4 m. The greater sampling depth in Krono¨ren was used due to the lack of perennial species in shallow areas, which is a result of the 4 months of ice cover every year (Kautsky, 1989), when ice scrapes off the large perennial fucoids. Hence, it is only at greater depths (3e4 m) that Fucus radicans is belt forming, reaching a cover of 25e75%. Not only does the depth distribution of the upper parts of the fucoid belt differ between the 2 investigated areas, but also do factors such as wave exposure, salinity, nutrient level and algal and faunal species. Since the depth distribution of the upper parts of the fucoid belt is only one of the many parameters that differs between the areas, we decided to investigate the upper parts of the fucoid belts, even though this resulted in different sampling depths. All sites in a single area (i.e., Krono¨ren or Asko¨) were sampled over 2 days, and the time gap between sampling the areas was 1 week. All samples were frozen to preserve them for further analysis. In the laboratory, samples were sorted, the fauna (>1 mm) counted, and the algae and fauna identified to the nearest possible taxa (species, genus or family level) and dried at 60 C to constant dry weight. The abundance and biomass of fauna were standardized to individuals m2 and g dry weight m2, respectively; the biomass of algae was standardized to g dry weight m2. The Shannon index of diversity (H0 ) was also calculated for the faunal community using abundance as the unit. This formula has 2 components, ‘‘taxa richness’’ and ‘‘equitability’’, and either an increase in the number of taxa or a more equal distribution of the abundance can result in higher index values (Lloyd and Gelhardi, 1964). 2.3. Statistical analysis Differences in Shannon diversity index (H0 ), faunal abundance and biomass as well as filamentous algae biomass in
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the 2 vegetation types were analysed using two-way ANOVA, analysing each region separately. Vegetation type (Fucoids and Non-fucoids) was used as a fixed factor and site (n ¼ 5) as a random factor. Pairwise comparisons between sites were made using Tukey’s honestly significantly different (HSD) test (significant p-value < 0.05). The biomass measurements of algae and the abundance measurements of fauna were square-root transformed (þ10) to achieve homogeneity of variance. All univariate tests were performed using Statistica 6.1. Differences in the composition of faunal abundance between the vegetation types were plotted using non-metric multidimensional scaling (nMDS) based on the Bray Curtis similarity index. Differences between ‘‘vegetation type’’ and ‘‘site’’ were tested using analysis of similarities (ANOSIM) with the two-way crossed design (PRIMER 5.0). To assess the contribution of different species to the differences between vegetation types, we applied similarity percentages for species contributions (SIMPER, PRIMER 5.0). Faunal abundances were square-root transformed in the multivariate analyses to reduce the influence of dominant species. The abundancee biomass comparison (ABC) curves were conduced using the PRIMER 5.0 software package. For each curve, the W value (which ranges from 1 to 1) was also calculated to represent each ABC plot in a single summary statistic: when W is positive, the biomass curve is above the abundance curve; when W is negative, the opposite occurs (Clarke and Warwick, 1994).
3. Results 3.1. Faunal composition Between 20 and 27 faunal taxa (identified to the species, genus or family level) were identified in the 2 different vegetation types (Fucoids and Non-fucoids) and areas (Krono¨ren and Asko¨). Most of these faunal taxa were represented in both vegetation types, whereas between 1 and 5 taxa, depending on the area and algal vegetation, were found only among the Fucoid or Non-fucoid vegetation. However, the Shannon index of diversity, H0 , for the faunal community in Krono¨ren indicated a significant interaction between vegetation type and site (Table 1), and the post doc test revealed a higher index for the Fucoid vegetation in 3 (K1eK3) of 5 investigated sites (Fig. 1A). No significant difference was, however, found between the algal vegetation types in Asko¨ (Fig. 1A, Table 1). Significant interactions were also found between vegetation type and site in terms of the number of faunal individuals m2 in both areas (Table 1). Post doc testing indicated a significantly greater abundance of fauna in Fucoid than in Nonfucoid vegetation in 1 (K3) of 5 sites in Krono¨ren and in 2 sites (A1eA2) in Asko¨ (Fig. 1B). When recalculating the fauna to biomass m2, significant interactions were also evident in both Krono¨ren and Asko¨ (Table 1). The post doc test for type of algal vegetation and site revealed greater biomass of fauna in the Fucoid than in the Non-fucoid vegetation in 4 of 5 sites (K1eK4) in Krono¨ren and in 3 sites (A1eA3) in Asko¨ (Fig. 1C).
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Table 1 Results of two-way ANOVAs testing differences in the Shannon index of diversity and number of fauna, as well as in biomass of fauna and filamentous algae between vegetation types (i.e., Fucoids and Non-fucoids) and sites in the Krono¨ren and Asko¨ study areas (n ¼ 6). The fucoid species is Fucus radicans in Krono¨ren and F. vesiculosus in Asko¨ Source of variation
Krono¨ren Effect
Asko¨ df
F
MS
Shannon index for fauna community Vegetation type Fixed Site Random Vegetation type site Random Residual
1 4 4 50
No. of fauna individuals m2 Vegetation type Site Vegetation type site Residual
Fixed Random Random
1 4 4 50
2220 1470 432 97.1
Biomass of fauna m2 Vegetation type Site Vegetation type site Residual
Fixed Random Random
1 4 4 50
3440 216 131 35.4
Biomass of filamentous algae m2 Vegetation type Fixed Site Random Vegetation type site Random Residual
1 4 4 50
2.44 0.14 0.26 0.06
232 3.56 4.90 1.19
The abundanceebiomass comparison plots for the different vegetation types and areas illustrate the different statistical outcomes in terms of abundance and biomass of fauna m2 (Fig. 2). In the Fucoid vegetation in Krono¨ren, the abundance was only significantly greater than in the Non-fucoid vegetation in 1 of 5 sites, whereas the biomass value was greater in 4 of 5 sites. This difference in consistency between these 2 measurements is illustrated in Fig. 2A, where the biomass curve for the Fucoids is above, while the corresponding curve for the Non-fucoids is below, the abundance curve. The measured abundance and biomass of fauna m2 in the different algal vegetation types in Asko¨ were, however, rather consistent, 2 and 3 sites of 5 having greater abundance and biomass, respectively, in the Fucoid than in the Non-fucoid vegetation. This pattern is displayed in Fig. 2B, where the abundancee biomass comparison plots depict similar patterns for the Fucoids and Non-fucoids, the biomass curves being below the abundance curves in both cases. The ordination of the nMDS indicated that the faunal samples from Fucoids and Non-fucoids in Krono¨ren formed 2 distinct groups (Fig. 3A). The pattern in Asko¨ was less obvious, the fauna samples from the Fucoids assembling in one group while the samples from the Non-fucoids formed a less distinct group (Fig. 3B). The vegetation types were significantly dissimilar at both Krono¨ren ( p < 0.001, R-value 0.95, ANOSIM) and Asko¨ ( p < 0.001, R-value 0.61, ANOSIM), although the 2 vegetation types were more distinct in Krono¨ren. The sampling sites in each area were also significantly different (Krono¨ren ¼ p < 0.001, R-value 0.60, Asko¨ ¼ p < 0.001, R-value 0.54, ANOSIM), and pairwise tests indicated that all sites differed from each other. The similarity percentages (SIMPER) of species contributions revealed an average dissimilarity of 62% between the
p
F
MS
0.56 9.50 4.24
ns 0.037 0.005
5.15 3.40 4.45
ns ns 0.004
30800 6340 2370 634
13.0 2.68 3.73
0.023 ns 0.010
0.007 ns 0.01
10250 1030 710 77.6
14.4 1.44 9.15
0.019 ns <0.001
17.4 22.5 0.85
0.014 0.005 ns
130 130 35.4
47.4 0.73 4.10
0.002 ns 0.006
0.02 0.07 0.06 0.07
86.6 112 4.98 5.87
1.11 0.34 0.92
p ns ns ns
2 vegetation types in Krono¨ren, whereas the vegetation types in Asko¨ displayed a lower value of 51%. In both areas, 13 faunal taxa contributed 95% of the dissimilarity between the fucoids and filamentous algal vegetation types (Table 2). 3.2. Filamentous algal composition In Krono¨ren, 18 filamentous algal taxa (species, genus or family level) were recorded growing epilithically, and 10 of these taxa were also found as epiphytes on Fucus radicans. The corresponding values for the algal vegetation in Asko¨ were 15 taxa, 8 of these growing as epiphytes on Fucus vesiculosus. The biomass of filamentous algae in the Fucoid vegetation in Krono¨ren was significantly lower than the biomass of algae in the corresponding Non-fucoid vegetation (Fig. 1D, Table 1). This significant interaction also indicated that the biomass of filamentous algae in Non-fucoids was significantly greater in K5 than in K4. The biomass of filamentous algae displayed a completely different pattern for the 2 algal vegetation types in Asko¨, where the biomass of filamentous algae m2 was significantly higher in the Fucoid than in the Non-fucoid vegetation (Table 1). Post doc testing for the different sites did not, however, reveal any specific significant differences between the 2 algal vegetations (Fig. 2D). The filamentous algal biomass also significantly differed between sites (Table 1). 4. Discussion The Fucoid vegetation in Krono¨ren (Fucus radicans) supported over a 3-times-greater total faunal biomass and the Fucoid vegetation in Asko¨ (Fucus vesiculosus) over a 3.5times-greater biomass than did nearby Non-fucoid vegetation.
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A
1.8
*
Shannon index (H')
1.6
***
253
Fucoids
*
Non-fucoids
1.4 1.2 1 0.8 0.6 0.4 0.2 0
B
25000
***
No of Fauna m-2
20000 15000
** 10000
***
5000 0
g dry wt of fauna m-2
C
70
***
60 50
***
40 30
***
***
***
**
20
***
10 0
g dry wt of filamentous algae m-2
D
300 250 200 150 100
***
*** ***
50
*
***
0 K1
K2
K3
K4
Kronören
K5
A1
A2
A3
A4
A5
Askö
Fig. 1. (A) The Shannon index of diversity, H0 , (B) number of faunal individuals m2, (C) biomass of macrofauna, g dry weight m2 and (D) biomass of filamentous algae, g dry weight m2, in the 5 study sites in Krono¨ren (K1eK5) and Asko¨ (A1eA5) and for the 2 algal vegetation types (Fucoids and Non-fucoids). The fucoid in Krono¨ren is Fucus radicans and in Asko¨ is F. vesiculosus. Figures display mean value SE (n ¼ 6). Asterisks indicate degree of significance determined by two-way ANOVAs and post doc tests (*p < 0.05, **p < 0.01, ***p < 0.001).
Thus, our results generally supported our hypothesis concerning the importance of a large structural perennial species for high invertebrate biomass production. However, statistical analysis indicated that the faunal biomass occurring in Fucoid versus Non-fucoid vegetation differed spatially, since significant interactions showed that the Fucoid community
harboured a greater faunal biomass in 4 and 3 of the 5 investigated sites in each of the Krono¨ren and Asko¨ study areas, respectively. The sites that contained significantly greater faunal biomass in the Fucoid vegetation were sites in the lower range of wave exposure, i.e., K1eK4 and A1eA3. This indicates that faunal composition differs depending on wave
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Fig. 2. Abundance and biomass plots for Fucoid and Non-fucoid algal vegetation in the (A) Krono¨ren and (B) Asko¨ areas. The species rank scale is logarithmic.
exposure, as has been demonstrated in previous studies of rocky shore communities (e.g., Fenwick, 1976; Bustamante and Branch, 1996). Fucoid vegetation stands in sheltered and semi-exposed sites might contain faunal species (such as the herbivorous snails Theodoxus fluviatilis and Radix
balthica) that would be easily detached from algal fronds and lost in wave-exposed sites. Additionally, both T. fluviatilis and R. balthica had higher abundance in the Fucoid vegetation in both areas. Hence, the higher faunal biomass in the Fucoids than in the Non-fucoids in K1eK4 and A1eA3 is suggested
Fig. 3. The ordinations from non-metric multidimensional scaling (nMDS) analyses of faunal composition in the Fucoid and Non-fucoid algal vegetations in Krono¨ren (A) and Asko¨ (B) from square-root transformed faunal abundance. The fucoid in Krono¨ren is Fucus radicans and in Asko¨ is F. vesiculosus. The different algal vegetation types form 2 distinct groups in Krono¨ren; the vegetation types in Asko¨ are less distinct.
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Table 2 Results of SIMPER analyses of the square-root transformed associated faunal composition, testing for differences between the Fucoid- (the fucoid species in Krono¨ren is F. radicans and in Asko¨ F. vesiculosus) and Non-fucoid vegetation. The 13 macrofauna taxa that accounted for 95% of the dissimilarity between the vegetation types are listed in order of decreasing importance. The values for mean number m2 (n ¼ 30) are from non-transformed data. Radix balthica was formerly known as Lymnaea peregra Krono¨ren
Mean number m2
Species
Fucoids
Non-fucoids
Gammarus spp. Chironomidae Jaera albifrons Theodoxus fluviatilis Radix balthica Macoma balthica Agraylea spp. Leptoceridae Hydrobiidae Argulus foliaceus Balanus improvisus Brachycentrus spp. Prostoma obscurum
1210 271 878 763 200 22.5 46.7 38.3 14.2 9.17 11.7 12.5 4.17
156 1610 2.5 163 131 98.3 19.2 13.3 10.0 7.50 1.67 e 10.0
Contrib.%
20.0 18.3 17.8 12.4 6.55 5.57 3.67 3.19 1.84 1.64 1.28 1.25 1.25
to represent the combined effect of a greater abundance of these gastropods in sheltered sites together with the overall greater abundance of these species in Fucoid vegetation. The greater faunal biomass m2 in F. vesiculosus than in filamentous algal vegetation has also been found in the southern Baltic Proper in localities at depths of 1 m with various wave exposures (Wikstro¨m and Kautsky, 2006). The same study also revealed a greater abundance of T. fluviatilis in F. vesiculosus vegetation (ca. 1500 m2 in F. vesiculosus versus ca. 500 m2 in filamentous algae) (Wikstro¨m and Kautsky, 2006). In contrast, Kraufvelin and Salovius (2004) detected no significant difference in faunal biomass m2 between the F. vesiculosus belt and the green alga Cladophora glomerata in the northern Baltic Proper, despite similar growing depths and wave exposures. Possibly, the lower abundance of the gastropod Hydrobiidae found in the F. vesiculous than in the C. glomerata belt, i.e., ca. 10 versus 900 individuals m2, resulted in a similar faunal biomass between the two investigated algal vegetations (Kraufvelin and Salovius (2004)). Similarly, the present study also found a lower abundance of Hydrobiidae in the Fucoid vegetation in Asko¨ than in the corresponding Non-fucoid vegetation, also in line with findings regarding comparable algal vegetation types in the southern part of the Baltic Proper (Wikstro¨m and Kautsky, 2006). The abundanceebiomass comparison (ABC) curves indicate different dominance patterns for the different types of algal vegetation in Krono¨ren, the faunal biomass curve for the Fucoids being above the abundance curve, while the corresponding curve for the Non-fucoid vegetation was below. ABC curves are based on the reK selection gradient, where ecological theories predict that K-strategist species of large body size and long lifespan will be dominant competitors under stable conditions (Warwick, 1986). In contrast, r-strategist species, which are opportunistic species possessing smaller bodies and shorter lifespans, are better competitors under disturbed conditions caused, for example, by pollution (Warwick, 1986) or habitat
Asko¨
Mean number m2
Species
Fucoids
Non-fucoids
Chironomidae Gammarus spp. Theodoxus fluviatilis Hydrobiidae Mytilus edulis Idotea baltica Palaemon adspersus Jaera albifrons Radix balthica Balanus improvisus Cottidae Idotea granulosa Cardium spp.
6110 3090 1180 69.2 85.0 37.5 16.7 10.0 10.0 24.2 0.83 8.33 8.33
2350 1640 284 302 15.8 8.33 0.83 11.7 4.17 0.83 7.50 e 5.83
Contrib.%
30.7 26.9 13.4 7.60 4.37 2.96 1.76 1.62 1.29 1.09 1.07 1.04 1.04
degradation (Casatti et al., 2006). Hence, when the biomass curve lies above the abundance curve, the community is dominated by K-strategist species, and, in the opposite scenario, by r-strategist species (Warwick, 1986). The difference in faunal biomass dominance between the 2 algal vegetation types in Krono¨ren is obviously not due to, for example, different pollution levels, but rather may result from the different structures of the algal species. Fucus radicans has broad fronds that are suitable for epibiont attachment. Concordantly were higher abundance of caddis fly species (Leptoceridae and Brachycentrus spp.) and barnacles (Balanus improvisus) more abundant in the Fucoid than in the Non-fucoid vegetation in Krono¨ren, being found attached to the F. radicans fronds. All these species incorporate relatively heavy ‘‘houses’’, which also contribute to the greater faunal biomass in the Fucoid vegetation. In contrast, larvae of the insect group Chironomidae, which contribute only slightly to overall biomass, were more abundant in the Nonfucoid than in the Fucoid vegetation in Krono¨ren. Since these insect larvae thrive in filamentous algae (e.g., Dubois et al., 2006), the difference in Chironomidae biomass between these 2 algal vegetation types may be due to the fact that the Fucoids in Krono¨ren harboured under one tenth the biomass of filamentous algae than did the Non-fucoids. These differences between the faunal communities in the Fucoid and Non-fucoid vegetation in Krono¨ren are in concordance with a study conducted in steams (Casatti et al., 2006). Habitats, which exhibited several kinds of disturbances, such as loss of canopy cover and mesohabitat simplification, revealed r-strategy dominance of the investigated fish assemblages, whereas undisturbed habitats showed K-strategy dominance (Casatti et al., 2006). Unlike the Fucoid vegetation in Krono¨ren, the Fucoids in Asko¨ harboured a greater biomass of filamentous algae m2 than did the Non-fucoid vegetation, which may have contributed to the greater abundance of Chironomidae in the Fucoid vegetation in the Asko¨ area. This pattern is mirrored in the ABC curves for the algal vegetation in Asko¨, where the faunal biomass curves were below the abundance curves for both algal vegetation types. Effluent discharge
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from pulp-mill (Warwick, 1986) and domestic sewage (Casatti et al., 2006) has earlier been shown to displace r-strategy dominance in faunal assemblages. The ongoing eutrophication in the Baltic Sea, including Asko¨ (Ro¨nnberg and Bonsdorff, 2004) may, hence, in part be responsible for the r-strategy dominance in the Fucoid as well as Non-fucoid vegetation in the present study. The Fucoid vegetation in Krono¨ren not only displayed K-strategy dominance in the ABC curves, but had also greater faunal diversity in the 3 most sheltered sites (K1eK3) than did the Non-fucoid vegetation as well as distinct seperated from the Non-fucoid vegetation in terms of nMDS ordination. In contrast, the algal vegetation in Asko¨ did not display any differences in terms of ABC curves or Shannon index (H0 ) values, and was not as distinct in the nMDS plot as was the algal vegetation in Krono¨ren. Furthermore, the different types of algal vegetation in Asko¨ displayed a lower average dissimilarity of species contributions (51%) than did corresponding vegetation types in Krono¨ren (62%). As mentioned earlier, a major difference between Fucoid vegetation in Krono¨ren and in Asko¨ is in the biomass of filamentous algae: Fucus radicans in Krono¨ren are almost totally free of filamentous algae, whereas the Fucus vesiculosus in the nutrient-enriched Asko¨ area has a high load of filamentous algal biomass. This difference in the biomass of filamentous algae in the Fucoid vegetation may reflect the different degrees of eutrophication occurring in the 2 areas, the Bothnian Sea (Krono¨ren) not being affected by nutrient enrichment, unlike the Baltic Proper (Asko¨) (Ro¨nnberg and Bonsdorff, 2004). Thus, the greater diversity of faunal composition found in 3 of 5 investigated sites in the Fucoid compared to the Non-fucoid vegetation, as well as the K-strategy curve (shown for the fauna measurements), may indicate a diverse fucoid community not influenced by nutrient enrichment and eutrophication. However, differing nutrient levels are only one of the many parameters that differ between the investigated areas. Additional abiotic factors that may have an impact on the associated fauna in Krono¨ren and Asko¨ are depth, wave exposure, salinity and temperature; as well, there are the biotic factors, i.e., the different Fucus species themselves. One of the factors that thus also may have contributed to the greater dissimilarities between the Fucoid and Non-fucoid vegetation in Krono¨ren than in Asko¨ is the different sampling depths (4 m in Krono¨ren and 0.4 m in Asko¨). This, in turn, also resulted in different wave exposures (the Ez values for the sites in Krono¨ren were between 0.04 and 0.15, whereas the corresponding values for Asko¨ were 0.60e3.90). More sediments and organic matter accumulate along sheltered shores (Prathep et al., 2003) and at greater depths, and sediments are also more easily trapped in filamentous algae than in fucoids (Eriksson and Johansson, 2003). Since detritivores have been demonstrated to be positively correlated with sediment accumulation in algal turfs (Prathep et al., 2003), a greater abundance of deposit feeders and/or detritivores may be expected to be found in the Non-fucoid vegetation in Krono¨ren. In accordance with this hypothesis, deposit feeders like Macoma balthica and Chironomidae (Johnson, 1985), (even though the latter also may contain species that are herbivores
or predators (Cuker, 1983)) were more abundant in the Nonfucoid than in the Fucoid vegetation in Krono¨ren. Earlier field studies at Ask (Haage, 1975) have recorded sparse populations of M. balthica in Fucus vesiculosus vegetation, and the abundance correlated with F. vesiculosus stands that had a thick layer of detritus and sediment or were surrounded by softbottom environments. The greater differences between the 2 algal vegetation types in Krono¨ren than between the corresponding vegetation types in Asko¨ may indicate that the fucoid and filamentous algal vegetations in deeper parts of the littoral zone differ more in ecological function than do the same vegetation types in shallower parts. Thus, a shift from fucoid to filamentous algal vegetation would be expected to have a greater impact on faunal composition in deeper parts of the algal belt. Additionally, a shift is more likely to occur in deeper parts of the littoral zone, since the depth distribution of F. vesiculosus has declined due to reduced light availability (Kautsky et al., 1986), and studies have found that increased sediment deposition inhibits the recruitment success of F. vesiculosus (Berger et al., 2003; Eriksson and Johansson, 2003). It has also been found that F. vesiculosus may be positively affected by wave movement through the reduction of sediments and drift algae (Roos et al., 2004), an effect that is likely to decrease with depth. As Fucus radicans is not belt forming at depths less than 3e4 m in the northern Bothnian Sea, a shift in the depth extension of F. radicans in this area could eliminate the whole fucoid population. On the other hand, in the Baltic Sea, recolonization of the deeper parts of the F. vesiculosus belt, after a shift to filamentous algae, could be supported by shallowwater F. vesiculosus stands. 5. Concluding remarks This study has demonstrated that the small and lessinvestigated fucoid species Fucus radicans may be as important as the larger Fucus vesiculosus, since both Fucoid vegetation types harboured significantly greater faunal biomasses m2 in 3e4 of 5 investigated sites than did the corresponding Non-fucoid vegetation. These sites were in the lower range of wave exposure studied, indicating the Fucoid vegetations’ important role in sheltered coastal areas. Additionally, in the most sheltered sites, the diversity index for faunal communities in Krono¨ren was significantly higher in the Fucoid compared to the Non-fucoid vegetations. The faunal abundance did, however, not differ in any considerable way due to high number of fauna with low biomass associated with the load of filamentous algae. Furthermore, specific faunal species may also be negatively affected by a shift from fucoids to filamentous algae since, for example, a greater abundance of the sessile barnacle Balanus improvisus was found in the Fucoid vegetation in both areas. This species probably benefits from the fucoids’ broad fronds, which may also be important for the caddis fly Brachycentrus spp. This Trichoptera larva was only found in the Fucoid vegetation in Krono¨ren and its tubes were made entirely of pieces of F. radicans (pers. obs.). Furthermore, the abundances of, for example, Idotea baltica in the Asko¨ area and Gammarus spp. and Theodoxus fluviatilis
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in both investigated areas were 5 to 8 times higher in the Fucoid vegetation. Thus, we suggest that a shift from fucoids to filamentous algal vegetation may not only change the biodiversity and function of the associated invertebrates, but may also have an impact on fish species such as perch (Perca fluviatilis), a common species in coastal areas of the Baltic Sea (Nilsson et al., 2004), which is known to prey on these invertebrates (Mattila, 1992; Lappalainen et al., 2001). Acknowledgments We are especially grateful to Patrik Dinnetz for his advice on statistical matters. We would also like to thank Susanne Qvarfordt for her diving assistance, Stefan Lundberg at the Museum of Natural History of Stockholm for identification of the freshwater faunal species, Sofia Wikstro¨m and Lena Bergstro¨m for valuable comments on the manuscript and Patrik Kraufvelin for discussion of statistical and scientific matters. We also want to thank 3 anonymous referees for comments that greatly benefited this manuscript. The study was performed as part of the MARBIPP programme, financed by the Swedish Environmental Protection Agency and by the Stockholm and the Umea˚ Marine Research Centres. References Alley, R.B., Marotzke, J., Nordhaus, W.D., Overpeck, J.T., Peteet, D.M., Pielke, R.A., Pierrehumbert, R.T., Rhines, P.B., Stocker, T.F., Talley, L.D., Wallace, J.M., 2003. Abrupt climate change. Science 299, 2005e2010. Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P.S., Airoldi, L., Relini, G., Cinelli, F., 2001. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Marine Ecology Progress Series 214, 137e150. 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. Bergstro¨m, L., Tatarenkov, A., Johannesson, K., Jo¨nsson, R.B., Kautsky, L., 2005. Genetic and morphological identification of Fucus radicans sp. nov. (Fucales, Phaeophyceae) in the brackish Baltic Sea. Journal of Phycology 41, 1025e1038. Bonsdorff, E., Blomquist, E.A., Mattila, J., Norkko, A., 1997. Coastal eutrophication: causes, consequences and perspectives in the Archipelago areas of the northern Baltic Sea. Estuarine, Coastal and Shelf Science 44 (Suppl. A), 63e72. Bustamante, R.H., Branch, G.M., 1996. Large scale patterns and trophic structure of southern African rock shores: the roles of geographic variation and wave exposure. Journal of Biogeography 23, 339e351. Casatti, L., Langeani, F., Ferreira, C.P., 2006. Effects of physical habitat degradation on the stream fish assemblage structure in a pasture region. Environmental Management 38, 974e982. Clarke, K.R., Warwick, R.M., 1994. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory, Plymouth, UK, 144 pp. Cederwall, H., Elmgren, R., 1990. Biological effects of eutrophication in the Baltic Sea, particularly the coastal zone. Ambio 19, 109e112. Cuker, B.E., 1983. Competition and coexistence among the grazing snail Lymnaea, Chironomidae, and microcrustacea in an arctic epilithic lacustrine community. Ecology 64, 10e15. Dubois, S., Commito, J.A., Olivier, F., Retie`re, C., 2006. Effects of epibionts on Sabellaria alveolata (L.) biogenic reefs and their associated fauna in the Bay of Mont Saint-Michel. Estuarine, Coastal and Shelf Science 68, 635e646.
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Eriksson, B.K., Johansson, G., Snoeijs, P., 1998. Long-term changes in the sublittoral zonation of brown algae in the southern Gulf of Bothnia. European Journal of Phycology 33, 241e249. Eriksson, B.K., Johansson, G., 2003. Sedimentation reduces recruitment success of Fucus vesiculosus (Phaeophyceae) in the Baltic Sea. European Journal of Phycology 38, 217e222. Fenwick, G.D., 1976. The effect of wave exposure on the amphipod fauna of the alga Caulerpa brownii. Journal of Experimental Marine Biology and Ecology 25, 1e18. Guidetti, P., Terlizzi, A., Fraschetti, S., Boero, F., 2003. Changes in Mediterranean rocky-reef fish assemblages exposed to sewage pollution. Marine Ecology Progress Series 253, 269e278. Haage, P., 1975. Quantitative investigations of the Baltic Fucus belt macrofauna: 2. Quantitative seasonal fluctuations. In: Contributions from the Asko¨ Lab. No. 10. University of Stockholm, Sweden, 88 pp. Hagerman, L., 1966. The macro- and microfauna associated with Fucus serratus L., with some ecological remarks. Ophelia 3, 1e43. Ha˚kansson, L., 1981. A Manual for Lake Morphometry. Springer-Verlag, Berlin, 78 pp. den Hartog, C., Polderman, P.J.G., 1975. Changes in the seagrass populations of the Dutch Waddenzee. Aquatic Botany 1, 141e147. Johnson, R.K., 1985. Feeding efficiencies of Chironomus plumosus (L.) and C. anthracinus Zett. (Diptera: Chironomidae) in mesotrophic Lake Erken. Freshwater Biology 15, 605e612. ˚ ., Salemaa, H., 1982. Kangas, P., Autio, H., Ha¨llfors, G., Luther, H., Niemi, A A general model of the decline of Fucus vesiculosus at Tva¨rminne, south coast of Finland in 1977e81. Acta Botanica Fennica 118, 1e27. Kautsky, H., 1989. Quantitative distribution of plant and animal communities of the phytobenthic zone in the Baltic Sea. In: Contributions from the Asko¨ Lab. No. 35. University of Stockholm, Sweden, 88 pp. Kautsky, H., Kautsky, L., Kautsky, N., Kautsky, U., Lindblad, C., 1992. Studies on the Fucus vesiculosus community in the Baltic Sea. Acta Phytogeographica Suecica 78, 33e48. Kautsky, N., Kautsky, H., Kautsky, U., Waern, M., 1986. Decreased depth penetration of Fucus vesiculosus (L.) since the 1940’s indicates eutrophication of the Baltic Sea. Marine Ecology Progress Series 28, 1e8. Kotta, J., Paalme, T., Martin, G., Ma¨kinen, A., 2000. Major changes in macroalgae community composition affect the food and habitat preference of Idotea baltica. International Review of Hydrobiology 85, 697e705. Kraufvelin, P., Salovius, S., 2004. Animal diversity in Baltic rocky shore macroalgae: can Cladophora glomerata compensate for lost Fucus vesiculosus? Estuarine, Coastal and Shelf Science 61, 369e378. Krause-Jensen, D., Carstensen, J., Dahl, K., 2007. Total and opportunistic algal cover in relation to environmental variables. Marine Pollution Bulletin 55, 114e125. Lappalainen, A., Rask, M., Koponen, H., Vesala, S., 2001. Relative abundance, diet and growth of perch (Perca fluviatilis) and roach (Rutilus rutilus) at Tva¨rminne, northern Baltic Sea, in 1975 and 1997: responses to eutrophication? Boreal Environment Reseach 6, 107e118. Leppa¨koski, E., Helminen, H., Ha¨nninen, J., Tallqvist, M., 1999. Aquatic biodiversity under anthropogenic stress: an insight from the Archipelago Sea (SW Finland). Biodiversity and Conservation 8, 55e70. Lloyd, M., Gelhardi, R.J., 1964. A table for calculating the ‘‘equitability’’ component of species diversity. Journal of Animal Ecology 33, 217e225. Mattila, J., 1992. Seasonal and spatial variation in the diet of perch (Perca fluviatilis L.) in a shallow soft-bottom area (SW Finland). In: Bjørnestad, E., Hagerman, L., Jensen, K. (Eds.), Proceedings of the 12th Baltic Marine Biologists Symposium. Olsen and Olsen, Fredensborg, pp. 101e107. Milazzo, M., Chemello, R., Badalamenti, F., Riggio, S., 2002. Short-term effect of human trampling on the upper infralittoral macroalgae of Ustica Island MPA (western Mediterranean, Italy). Journal of Marine Biological Association of the United Kingdom 82, 745e748. Nilsson, J., Anersson, J., Kara˚s, P., Sandstro¨m, O., 2004. Recruitment failure and decreasing catches of perch (Perca fluviatilis L.) and pike (Esox lucius L.) in the coastal waters of southeast Sweden. Boreal Environmental Research 9, 295e306.
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Omstedt, A., Hansson, D., 2006. The Baltic Sea ocean climate system memory and response to changes in the water and heat balance components. Continental Shelf Research 26, 236e251. Pedersen, M.F., 1995. Nitrogen limitation of photosynthesis and growth: comparison across aquatic plant communities in a Danish estuary (Roskilde Fjord). Ophelia 41, 261e272. Prathep, A., Marrs, R.H., Norton, T.A., 2003. Spatial and temporal variations in sediment accumulation in an algal turf and their impact on associated fauna. Marine Biology 142, 381e390. Pihl, L., Wennhage, H., Nilsson, S., 1994. Fish assemblage structure in relation to macrophytes and filamentous epiphytes in shallow non-tidal rock-bottom and soft-bottom habitats. Environmental Biology of Fishes 39, 271e288. Reed, B.J., Hovel, K.A., 2006. Seagrass habitat disturbance: how loss and fragmentation of eelgrass Zostera marina influences epifaunal abundance and diversity. Marine Ecology Progress Series 326, 133e143. Roos, C., Ro¨nnberg, O., Berglund, J., Alm, A., 2004. Long-term changes in macroalgal communities along ferry routes in a northern Baltic Archipelago. Nordic Journal of Botany 23, 247e259. Ro¨nnberg, C., Bonsdorff, E., 2004. Baltic Sea eutrophication: area-specific ecological consequences. Hydrobiologia 514, 227e241. Tatarenkov, A., Bergstro¨m, L., Jo¨nsson, B., Serr~ao, E.A., Kautsky, L., Johannesson, K., 2005. Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Molecular Ecology 14, 647e651.
Terrados, J., Duarte, C.M., Fortes, M.D., Borum, J., Agawin, N.S.R., Bach, S., Thampanya, U., Kamp-Nielsen, L., Kenworthy, W.J., Geertz-Hansen, O., Vermaat, J., 1998. Changes in community structure and biomass of seagrass communities along gradients of siltation in SE Asia. Estuarine, Coastal and Shelf Science 46, 757e768. Vogt, H., Schramm, W., 1991. Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Marine Ecology Progress Series 69, 189e194. Wallentinus, I., 1978. Environmental influences on benthic macrovegetation in the TrosaeAsko¨ area, Northern Baltic Proper: I. Hydrographical and chemical parameters, and the macrophytic communities. In: Contributions from the Asko¨ Lab. No. 15. University of Stockholm, Sweden, 138 pp. Warwick, R.M., 1986. A new method for detecting pollution effects on marine macrobenthic communities. Marine Biology 92, 557e562. Wikstro¨m, S.A., Kautsky, L., 2006. Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuarine, Coastal and Shelf Science. doi:10.1016/ j.ecss.2006.10.009. Worm, B., Lotz, H.K., Bostro¨m, C., Engkvist, R., Labanauskas, V., Sommer, U., 1999. Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Marine Ecology Progress Series 185, 309e314.
A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae Sonja Ra˚berg*, Lena Kautsky Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden Received 19 September 2006; accepted 12 January 2007 Available online 7 March 2007
Abstract Anthropogenic activities worldwide have contributed to vegetation changes in many coastal areas, changes that may in turn affect faunal and algal assemblages in the involved ecosystems. In the northernmost part of the Baltic Sea the salinity is extremely low (3e4) and the only structurally complex alga present is Fucus radicans. Since in this area F. radicans is living at its salinity tolerance limit, it is potentially very sensitive to environmental changes. Any change in salinity could thus alter the overall algal community, changing it to one dominated solely by filamentous algae. To determine the importance of F. radicans to the associated faunal community, we examined differences between the 2 main vegetation types present, i.e., F. radicans and filamentous algae, in the Krono¨ren marine reserve in the northernmost part of the Baltic Sea. A similar study was conducted in the Asko¨ area in the northern Baltic Proper, where the more-investigated Fucus vesiculosus is the only large fucoid present. The biomass of associated fauna was significantly higher in both the F. radicans and F. vesiculosus than in the filamentous algal vegetation at some, but not all, sites. The F. radicans community also displayed a greater diversity of associated fauna in 3 of 5 investigated Krono¨ren sites, whereas no difference in diversity was detected between F. vesiculosus and the filamentous algal vegetations in the Asko¨ sites. Furthermore, the F. radicans community displayed a different faunal community, being the only investigated algal community with a faunal community dominated by K-strategy species, according to abundanceebiomass comparison curves. This pattern may be due to the low epiphytic load on these Fucus plants. In contrast, the F. vesiculosus community, as well as the algal communities with no Fucus in both areas, had high biomasses of filamentous algae and an invertebrate fauna dominated by Chironomidae, occurring in great abundance but only with a low biomass. ANOSIM analyses of faunal composition demonstrated a significant difference between the 2 vegetation types in both areas, largely due to greater abundance of Gammarus spp. and Theodoxus fluviatilis in the fucoid vegetation. Differences observed between the F. radicans and filamentous algal vegetation types were generally more pronounced than those between F. vesiculosus and nearby filamentous algal vegetation. These observations may be due to abiotic factors that differ between the 2 investigated areas, factors such as depth distribution, wave action and eutrophication level. This study has demonstrated that the less-investigated F. radicans may be as important as the larger F. vesiculosus for the associated faunal assemblages. At the same time, the limited extent of F. radicans at shallower depths makes F. radicans vegetation potentially more vulnerable to anthropogenic changes, as declines in fucoid vegetation are usually first manifested in populations at their lower depth limits, whereas shallow populations are less affected. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Fucus radicans; Fucus vesiculosus; biodiversity; species composition; Baltic Sea; Baltic Proper; Bothnian Sea
1. Introduction Human activities are believed to have had major impacts on vegetation composition in coastal areas. For example, human * Corresponding author. E-mail address: [email protected] (S. Ra˚berg). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.01.005
trampling on rocky shores in the Mediterranean has decreased both algal cover and the canopy of dominant macroalgal species (Milazzo et al., 2002). Furthermore, seagrass communities in the tropics have been shown to have been indirectly affected by anthropogenic activities such as rapid deforestation, which increases the siltation of coastal ecosystems (Terrados et al., 1998). Moreover, pollution together with the outbreak of
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‘‘wasting disease’’ has been responsible for a large decline in eelgrass populations (den Hartog and Polderman, 1975). Changes in the abundance and/or composition of macrophytes, such as those listed above, may in turn affect other organisms in an ecosystem by altering associated invertebrate communities (Benedetti-Cecchi et al., 2001; Reed and Hovel, 2006; Wikstro¨m and Kautsky, 2006) as well as fish assemblages (Pihl et al., 1994; Guidetti et al., 2003). Shifts from macroalgal to filamentous algal species are also believed not only to reduce the availability of resources, such as food and shelter, for small faunal species such as crustaceans, but also to have additional negative effects on food webs by, for example, altering nutrient storage and reducing the nursery areas and prey of fishes (Kangas et al., 1982; Kautsky et al., 1992). The newly described canopy-forming alga Fucus radicans sp. nov. (Bergstro¨m et al., 2005) is the dominant, large, structurally complex brown alga that tolerates the low salinity (3e4) in the northern Bothnian Sea (Baltic Sea). Fucus radicans differs morphologically from the common fucoid species Fucus vesiculosus by having no bladders, narrower fronds, a bushier appearance and being smaller in size (Bergstro¨m et al., 2005). The populations of F. radicans in the northern Bothnian Sea exist at their lower salinity range limit and are thus vulnerable to any further reduction in salinity. The increasing probability of abrupt climate change due to anthropogenic activities (Alley et al., 2003), therefore, threatens F. radicans, since rising air temperatures may enhance freshwater run-off and further lower Baltic Sea salinity (Omstedt and Hansson, 2006). The fact that F. radicans populations are largely (ca. 80%) clonal and hence, have low genetic variation (Bergstro¨m et al., 2005; Tatarenkov et al., 2005) further reduces its ability to cope with reduced salinity. Cover of opportunistic algal species is on the contrary positively correlated with decreasing salinity (Krause-Jensen et al., 2007). Despite numerous studies documenting the importance of structuring macrophytes for the diversity of associated fauna, no studies of which we are aware have investigated the significance of F. radicans for the faunal community inhabiting the algal belt. In contrast to Fucus radicans, the closely related species Fucus vesiculosus, which also inhabits the Baltic Sea, has declined in many areas since the 1970s (e.g., Kautsky et al., 1986; Vogt and Schramm, 1991; Eriksson et al., 1998; Kotta et al., 2000). Unlike the Bothnian Sea, the Baltic Proper is regarded as eutrophied (Ro¨nnberg and Bonsdorff, 2004), which in turn has resulted in the enhanced production of annual filamentous algae (e.g., Cederwall and Elmgren, 1990; Bonsdorff et al., 1997). The decline of F. vesiculosus and its replacement with filamentous algal species in this area (Leppa¨koski et al., 1999; Worm et al., 1999) may partly be due to an indirect effect of eutrophication, since high nitrogen levels favour the growth of these algae through their higher surface area:volume ratio (Pedersen, 1995). The ongoing decline in Fucus vesiculosus populations has prompted studies of the difference in biodiversity between the F. vesiculosus and the filamentous algal vegetation types that occupy similar habitats in the northern (Kraufvelin and Salovius, 2004) and southern (Wikstro¨m and Kautsky, 2006)
parts, respectively, of the Baltic Proper. These 2 studies, being somewhat different in approach, arrived at contradictory results. For example, greater faunal biomass was harboured by F. vesiculosus than by filamentous algal vegetation in the southern Baltic Proper (Wikstro¨m and Kautsky, 2006), while no such difference was detected in the northern Baltic Proper (Kraufvelin and Salovius, 2004). Furthermore, species richness was greater in the filamentous algal vegetation in the northern Baltic Proper than in the corresponding F. vesiculosus vegetation (Kraufvelin and Salovius, 2004), while no difference in species richness was detected between the vegetation types in the southern Baltic Proper (Wikstro¨m and Kautsky, 2006). The present study aims to investigate and compare the diversity, composition, abundance and biomass of the associated macrofauna (‘‘fauna’’) among stands of Fucus radicans and Fucus vesiculosus (‘‘Fucoids’’) versus among stands of corresponding filamentous algae (‘‘Non-fucoids’’). We hypothesized that the Fucoids would harbour a greater diversity, abundance and biomass of associated fauna m2. We also hypothesized that the faunal species composition would differ significantly between the 2 algal vegetation types in their respective regions. These potential differences are explored by using different multivariate analyses, one being k-dominance curves (Warwick, 1986) as an illustration of the abundance and biomass evenness among taxa. These curves are used to visually represent whether or not the faunal community is characterised by K- or r-selected taxa. Under ‘‘stable’’ conditions, K-selected taxa with the attributes of, for example, large body size and rather constant population size are the competitive dominants (Warwick, 1986). During pollution and/or habitat degradation, however, these taxa are less favoured and opportunistic r-selected species with, for example, small body size and highly variable population size are the numerical dominants (Warwick, 1986). Furthermore, we compared the biomasses of the filamentous algae m2 of both the Fucoid and Non-fucoid vegetation types, to control for the fact that, according to, for example, Hagerman (1966), faunal abundance is positively correlated with the amount of filamentous algae. 2. Materials and methods 2.1. Study sites The field studies were carried out in July 2003 at 5 sites in the Krono¨ren marine reserve, northern Bothnian Sea (63 260 N, 19 250 E), and 5 sites in the Asko¨ area, northern Baltic Proper (58 490 N, 19 390 E). The sampled sites were within 5 km of each other and varied in terms of wave exposure. Wave exposure at each site was calculated as thePmaximum local fetch P using the formula Lf ¼ ( ci cos gi)/( cos gi), where Lf is the maximum local fetch (wave exposure) and ci is the distance in kilometers to the nearest land (Ha˚kansson, 1981). The distance was measured in 15 directions with deviation angles ( gi) of 6, 12, 18, 24, 30, 36 and 42 from a central radius and in the direction of the transect. The exposure was corrected for depth according to the formula Ez ¼ E0 ez, where E0 is the degree of exposure at
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the surface and Ez the degree of exposure at a depth of z meters. The sites are referred to as K1eK5 in Krono¨ren and A1eA5 in Asko¨, 1 being the most sheltered site and 5 the most exposed. The Ez values for the sites varied between 0.04 and 0.15 and 0.60 and 3.90 in Krono¨ren and Asko¨, respectively. Samples were collected from hard substrates (rocks or large boulders). The salinity at sampling, measured using the Practical Salinity Scale, was 4.5 in Krono¨ren, but can vary between 3.5 and 5 (Kautsky, 1989). The salinity in the Asko¨ area varies between 5.8 and 7 (Wallentinus, 1978) but was approximately 6 at the time of sampling. The Krono¨ren marine reserve in northern Bothnian Sea will hereafter be referred to simply as ‘‘Krono¨ren’’, while the Asko¨ area in the northern Baltic Sea will be referred to as ‘‘Asko¨’’. 2.2. Data collection and treatment A 0.2 m2 frame with attached net bag (1 mm mesh size) was used to collect samples of a standardized size. Six replicates were randomly sampled in patches with and without fucoids at each site, in the upper parts of the fucoid belt where the fucoid cover was approximately 60% with small variations between sites and areas. In Krono¨ren, samples were taken at a depth of approximately 4 m and in Asko¨ at 0.4 m. The greater sampling depth in Krono¨ren was used due to the lack of perennial species in shallow areas, which is a result of the 4 months of ice cover every year (Kautsky, 1989), when ice scrapes off the large perennial fucoids. Hence, it is only at greater depths (3e4 m) that Fucus radicans is belt forming, reaching a cover of 25e75%. Not only does the depth distribution of the upper parts of the fucoid belt differ between the 2 investigated areas, but also do factors such as wave exposure, salinity, nutrient level and algal and faunal species. Since the depth distribution of the upper parts of the fucoid belt is only one of the many parameters that differs between the areas, we decided to investigate the upper parts of the fucoid belts, even though this resulted in different sampling depths. All sites in a single area (i.e., Krono¨ren or Asko¨) were sampled over 2 days, and the time gap between sampling the areas was 1 week. All samples were frozen to preserve them for further analysis. In the laboratory, samples were sorted, the fauna (>1 mm) counted, and the algae and fauna identified to the nearest possible taxa (species, genus or family level) and dried at 60 C to constant dry weight. The abundance and biomass of fauna were standardized to individuals m2 and g dry weight m2, respectively; the biomass of algae was standardized to g dry weight m2. The Shannon index of diversity (H0 ) was also calculated for the faunal community using abundance as the unit. This formula has 2 components, ‘‘taxa richness’’ and ‘‘equitability’’, and either an increase in the number of taxa or a more equal distribution of the abundance can result in higher index values (Lloyd and Gelhardi, 1964). 2.3. Statistical analysis Differences in Shannon diversity index (H0 ), faunal abundance and biomass as well as filamentous algae biomass in
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the 2 vegetation types were analysed using two-way ANOVA, analysing each region separately. Vegetation type (Fucoids and Non-fucoids) was used as a fixed factor and site (n ¼ 5) as a random factor. Pairwise comparisons between sites were made using Tukey’s honestly significantly different (HSD) test (significant p-value < 0.05). The biomass measurements of algae and the abundance measurements of fauna were square-root transformed (þ10) to achieve homogeneity of variance. All univariate tests were performed using Statistica 6.1. Differences in the composition of faunal abundance between the vegetation types were plotted using non-metric multidimensional scaling (nMDS) based on the Bray Curtis similarity index. Differences between ‘‘vegetation type’’ and ‘‘site’’ were tested using analysis of similarities (ANOSIM) with the two-way crossed design (PRIMER 5.0). To assess the contribution of different species to the differences between vegetation types, we applied similarity percentages for species contributions (SIMPER, PRIMER 5.0). Faunal abundances were square-root transformed in the multivariate analyses to reduce the influence of dominant species. The abundancee biomass comparison (ABC) curves were conduced using the PRIMER 5.0 software package. For each curve, the W value (which ranges from 1 to 1) was also calculated to represent each ABC plot in a single summary statistic: when W is positive, the biomass curve is above the abundance curve; when W is negative, the opposite occurs (Clarke and Warwick, 1994).
3. Results 3.1. Faunal composition Between 20 and 27 faunal taxa (identified to the species, genus or family level) were identified in the 2 different vegetation types (Fucoids and Non-fucoids) and areas (Krono¨ren and Asko¨). Most of these faunal taxa were represented in both vegetation types, whereas between 1 and 5 taxa, depending on the area and algal vegetation, were found only among the Fucoid or Non-fucoid vegetation. However, the Shannon index of diversity, H0 , for the faunal community in Krono¨ren indicated a significant interaction between vegetation type and site (Table 1), and the post doc test revealed a higher index for the Fucoid vegetation in 3 (K1eK3) of 5 investigated sites (Fig. 1A). No significant difference was, however, found between the algal vegetation types in Asko¨ (Fig. 1A, Table 1). Significant interactions were also found between vegetation type and site in terms of the number of faunal individuals m2 in both areas (Table 1). Post doc testing indicated a significantly greater abundance of fauna in Fucoid than in Nonfucoid vegetation in 1 (K3) of 5 sites in Krono¨ren and in 2 sites (A1eA2) in Asko¨ (Fig. 1B). When recalculating the fauna to biomass m2, significant interactions were also evident in both Krono¨ren and Asko¨ (Table 1). The post doc test for type of algal vegetation and site revealed greater biomass of fauna in the Fucoid than in the Non-fucoid vegetation in 4 of 5 sites (K1eK4) in Krono¨ren and in 3 sites (A1eA3) in Asko¨ (Fig. 1C).
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Table 1 Results of two-way ANOVAs testing differences in the Shannon index of diversity and number of fauna, as well as in biomass of fauna and filamentous algae between vegetation types (i.e., Fucoids and Non-fucoids) and sites in the Krono¨ren and Asko¨ study areas (n ¼ 6). The fucoid species is Fucus radicans in Krono¨ren and F. vesiculosus in Asko¨ Source of variation
Krono¨ren Effect
Asko¨ df
F
MS
Shannon index for fauna community Vegetation type Fixed Site Random Vegetation type site Random Residual
1 4 4 50
No. of fauna individuals m2 Vegetation type Site Vegetation type site Residual
Fixed Random Random
1 4 4 50
2220 1470 432 97.1
Biomass of fauna m2 Vegetation type Site Vegetation type site Residual
Fixed Random Random
1 4 4 50
3440 216 131 35.4
Biomass of filamentous algae m2 Vegetation type Fixed Site Random Vegetation type site Random Residual
1 4 4 50
2.44 0.14 0.26 0.06
232 3.56 4.90 1.19
The abundanceebiomass comparison plots for the different vegetation types and areas illustrate the different statistical outcomes in terms of abundance and biomass of fauna m2 (Fig. 2). In the Fucoid vegetation in Krono¨ren, the abundance was only significantly greater than in the Non-fucoid vegetation in 1 of 5 sites, whereas the biomass value was greater in 4 of 5 sites. This difference in consistency between these 2 measurements is illustrated in Fig. 2A, where the biomass curve for the Fucoids is above, while the corresponding curve for the Non-fucoids is below, the abundance curve. The measured abundance and biomass of fauna m2 in the different algal vegetation types in Asko¨ were, however, rather consistent, 2 and 3 sites of 5 having greater abundance and biomass, respectively, in the Fucoid than in the Non-fucoid vegetation. This pattern is displayed in Fig. 2B, where the abundancee biomass comparison plots depict similar patterns for the Fucoids and Non-fucoids, the biomass curves being below the abundance curves in both cases. The ordination of the nMDS indicated that the faunal samples from Fucoids and Non-fucoids in Krono¨ren formed 2 distinct groups (Fig. 3A). The pattern in Asko¨ was less obvious, the fauna samples from the Fucoids assembling in one group while the samples from the Non-fucoids formed a less distinct group (Fig. 3B). The vegetation types were significantly dissimilar at both Krono¨ren ( p < 0.001, R-value 0.95, ANOSIM) and Asko¨ ( p < 0.001, R-value 0.61, ANOSIM), although the 2 vegetation types were more distinct in Krono¨ren. The sampling sites in each area were also significantly different (Krono¨ren ¼ p < 0.001, R-value 0.60, Asko¨ ¼ p < 0.001, R-value 0.54, ANOSIM), and pairwise tests indicated that all sites differed from each other. The similarity percentages (SIMPER) of species contributions revealed an average dissimilarity of 62% between the
p
F
MS
0.56 9.50 4.24
ns 0.037 0.005
5.15 3.40 4.45
ns ns 0.004
30800 6340 2370 634
13.0 2.68 3.73
0.023 ns 0.010
0.007 ns 0.01
10250 1030 710 77.6
14.4 1.44 9.15
0.019 ns <0.001
17.4 22.5 0.85
0.014 0.005 ns
130 130 35.4
47.4 0.73 4.10
0.002 ns 0.006
0.02 0.07 0.06 0.07
86.6 112 4.98 5.87
1.11 0.34 0.92
p ns ns ns
2 vegetation types in Krono¨ren, whereas the vegetation types in Asko¨ displayed a lower value of 51%. In both areas, 13 faunal taxa contributed 95% of the dissimilarity between the fucoids and filamentous algal vegetation types (Table 2). 3.2. Filamentous algal composition In Krono¨ren, 18 filamentous algal taxa (species, genus or family level) were recorded growing epilithically, and 10 of these taxa were also found as epiphytes on Fucus radicans. The corresponding values for the algal vegetation in Asko¨ were 15 taxa, 8 of these growing as epiphytes on Fucus vesiculosus. The biomass of filamentous algae in the Fucoid vegetation in Krono¨ren was significantly lower than the biomass of algae in the corresponding Non-fucoid vegetation (Fig. 1D, Table 1). This significant interaction also indicated that the biomass of filamentous algae in Non-fucoids was significantly greater in K5 than in K4. The biomass of filamentous algae displayed a completely different pattern for the 2 algal vegetation types in Asko¨, where the biomass of filamentous algae m2 was significantly higher in the Fucoid than in the Non-fucoid vegetation (Table 1). Post doc testing for the different sites did not, however, reveal any specific significant differences between the 2 algal vegetations (Fig. 2D). The filamentous algal biomass also significantly differed between sites (Table 1). 4. Discussion The Fucoid vegetation in Krono¨ren (Fucus radicans) supported over a 3-times-greater total faunal biomass and the Fucoid vegetation in Asko¨ (Fucus vesiculosus) over a 3.5times-greater biomass than did nearby Non-fucoid vegetation.
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A
1.8
*
Shannon index (H')
1.6
***
253
Fucoids
*
Non-fucoids
1.4 1.2 1 0.8 0.6 0.4 0.2 0
B
25000
***
No of Fauna m-2
20000 15000
** 10000
***
5000 0
g dry wt of fauna m-2
C
70
***
60 50
***
40 30
***
***
***
**
20
***
10 0
g dry wt of filamentous algae m-2
D
300 250 200 150 100
***
*** ***
50
*
***
0 K1
K2
K3
K4
Kronören
K5
A1
A2
A3
A4
A5
Askö
Fig. 1. (A) The Shannon index of diversity, H0 , (B) number of faunal individuals m2, (C) biomass of macrofauna, g dry weight m2 and (D) biomass of filamentous algae, g dry weight m2, in the 5 study sites in Krono¨ren (K1eK5) and Asko¨ (A1eA5) and for the 2 algal vegetation types (Fucoids and Non-fucoids). The fucoid in Krono¨ren is Fucus radicans and in Asko¨ is F. vesiculosus. Figures display mean value SE (n ¼ 6). Asterisks indicate degree of significance determined by two-way ANOVAs and post doc tests (*p < 0.05, **p < 0.01, ***p < 0.001).
Thus, our results generally supported our hypothesis concerning the importance of a large structural perennial species for high invertebrate biomass production. However, statistical analysis indicated that the faunal biomass occurring in Fucoid versus Non-fucoid vegetation differed spatially, since significant interactions showed that the Fucoid community
harboured a greater faunal biomass in 4 and 3 of the 5 investigated sites in each of the Krono¨ren and Asko¨ study areas, respectively. The sites that contained significantly greater faunal biomass in the Fucoid vegetation were sites in the lower range of wave exposure, i.e., K1eK4 and A1eA3. This indicates that faunal composition differs depending on wave
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Fig. 2. Abundance and biomass plots for Fucoid and Non-fucoid algal vegetation in the (A) Krono¨ren and (B) Asko¨ areas. The species rank scale is logarithmic.
exposure, as has been demonstrated in previous studies of rocky shore communities (e.g., Fenwick, 1976; Bustamante and Branch, 1996). Fucoid vegetation stands in sheltered and semi-exposed sites might contain faunal species (such as the herbivorous snails Theodoxus fluviatilis and Radix
balthica) that would be easily detached from algal fronds and lost in wave-exposed sites. Additionally, both T. fluviatilis and R. balthica had higher abundance in the Fucoid vegetation in both areas. Hence, the higher faunal biomass in the Fucoids than in the Non-fucoids in K1eK4 and A1eA3 is suggested
Fig. 3. The ordinations from non-metric multidimensional scaling (nMDS) analyses of faunal composition in the Fucoid and Non-fucoid algal vegetations in Krono¨ren (A) and Asko¨ (B) from square-root transformed faunal abundance. The fucoid in Krono¨ren is Fucus radicans and in Asko¨ is F. vesiculosus. The different algal vegetation types form 2 distinct groups in Krono¨ren; the vegetation types in Asko¨ are less distinct.
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255
Table 2 Results of SIMPER analyses of the square-root transformed associated faunal composition, testing for differences between the Fucoid- (the fucoid species in Krono¨ren is F. radicans and in Asko¨ F. vesiculosus) and Non-fucoid vegetation. The 13 macrofauna taxa that accounted for 95% of the dissimilarity between the vegetation types are listed in order of decreasing importance. The values for mean number m2 (n ¼ 30) are from non-transformed data. Radix balthica was formerly known as Lymnaea peregra Krono¨ren
Mean number m2
Species
Fucoids
Non-fucoids
Gammarus spp. Chironomidae Jaera albifrons Theodoxus fluviatilis Radix balthica Macoma balthica Agraylea spp. Leptoceridae Hydrobiidae Argulus foliaceus Balanus improvisus Brachycentrus spp. Prostoma obscurum
1210 271 878 763 200 22.5 46.7 38.3 14.2 9.17 11.7 12.5 4.17
156 1610 2.5 163 131 98.3 19.2 13.3 10.0 7.50 1.67 e 10.0
Contrib.%
20.0 18.3 17.8 12.4 6.55 5.57 3.67 3.19 1.84 1.64 1.28 1.25 1.25
to represent the combined effect of a greater abundance of these gastropods in sheltered sites together with the overall greater abundance of these species in Fucoid vegetation. The greater faunal biomass m2 in F. vesiculosus than in filamentous algal vegetation has also been found in the southern Baltic Proper in localities at depths of 1 m with various wave exposures (Wikstro¨m and Kautsky, 2006). The same study also revealed a greater abundance of T. fluviatilis in F. vesiculosus vegetation (ca. 1500 m2 in F. vesiculosus versus ca. 500 m2 in filamentous algae) (Wikstro¨m and Kautsky, 2006). In contrast, Kraufvelin and Salovius (2004) detected no significant difference in faunal biomass m2 between the F. vesiculosus belt and the green alga Cladophora glomerata in the northern Baltic Proper, despite similar growing depths and wave exposures. Possibly, the lower abundance of the gastropod Hydrobiidae found in the F. vesiculous than in the C. glomerata belt, i.e., ca. 10 versus 900 individuals m2, resulted in a similar faunal biomass between the two investigated algal vegetations (Kraufvelin and Salovius (2004)). Similarly, the present study also found a lower abundance of Hydrobiidae in the Fucoid vegetation in Asko¨ than in the corresponding Non-fucoid vegetation, also in line with findings regarding comparable algal vegetation types in the southern part of the Baltic Proper (Wikstro¨m and Kautsky, 2006). The abundanceebiomass comparison (ABC) curves indicate different dominance patterns for the different types of algal vegetation in Krono¨ren, the faunal biomass curve for the Fucoids being above the abundance curve, while the corresponding curve for the Non-fucoid vegetation was below. ABC curves are based on the reK selection gradient, where ecological theories predict that K-strategist species of large body size and long lifespan will be dominant competitors under stable conditions (Warwick, 1986). In contrast, r-strategist species, which are opportunistic species possessing smaller bodies and shorter lifespans, are better competitors under disturbed conditions caused, for example, by pollution (Warwick, 1986) or habitat
Asko¨
Mean number m2
Species
Fucoids
Non-fucoids
Chironomidae Gammarus spp. Theodoxus fluviatilis Hydrobiidae Mytilus edulis Idotea baltica Palaemon adspersus Jaera albifrons Radix balthica Balanus improvisus Cottidae Idotea granulosa Cardium spp.
6110 3090 1180 69.2 85.0 37.5 16.7 10.0 10.0 24.2 0.83 8.33 8.33
2350 1640 284 302 15.8 8.33 0.83 11.7 4.17 0.83 7.50 e 5.83
Contrib.%
30.7 26.9 13.4 7.60 4.37 2.96 1.76 1.62 1.29 1.09 1.07 1.04 1.04
degradation (Casatti et al., 2006). Hence, when the biomass curve lies above the abundance curve, the community is dominated by K-strategist species, and, in the opposite scenario, by r-strategist species (Warwick, 1986). The difference in faunal biomass dominance between the 2 algal vegetation types in Krono¨ren is obviously not due to, for example, different pollution levels, but rather may result from the different structures of the algal species. Fucus radicans has broad fronds that are suitable for epibiont attachment. Concordantly were higher abundance of caddis fly species (Leptoceridae and Brachycentrus spp.) and barnacles (Balanus improvisus) more abundant in the Fucoid than in the Non-fucoid vegetation in Krono¨ren, being found attached to the F. radicans fronds. All these species incorporate relatively heavy ‘‘houses’’, which also contribute to the greater faunal biomass in the Fucoid vegetation. In contrast, larvae of the insect group Chironomidae, which contribute only slightly to overall biomass, were more abundant in the Nonfucoid than in the Fucoid vegetation in Krono¨ren. Since these insect larvae thrive in filamentous algae (e.g., Dubois et al., 2006), the difference in Chironomidae biomass between these 2 algal vegetation types may be due to the fact that the Fucoids in Krono¨ren harboured under one tenth the biomass of filamentous algae than did the Non-fucoids. These differences between the faunal communities in the Fucoid and Non-fucoid vegetation in Krono¨ren are in concordance with a study conducted in steams (Casatti et al., 2006). Habitats, which exhibited several kinds of disturbances, such as loss of canopy cover and mesohabitat simplification, revealed r-strategy dominance of the investigated fish assemblages, whereas undisturbed habitats showed K-strategy dominance (Casatti et al., 2006). Unlike the Fucoid vegetation in Krono¨ren, the Fucoids in Asko¨ harboured a greater biomass of filamentous algae m2 than did the Non-fucoid vegetation, which may have contributed to the greater abundance of Chironomidae in the Fucoid vegetation in the Asko¨ area. This pattern is mirrored in the ABC curves for the algal vegetation in Asko¨, where the faunal biomass curves were below the abundance curves for both algal vegetation types. Effluent discharge
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from pulp-mill (Warwick, 1986) and domestic sewage (Casatti et al., 2006) has earlier been shown to displace r-strategy dominance in faunal assemblages. The ongoing eutrophication in the Baltic Sea, including Asko¨ (Ro¨nnberg and Bonsdorff, 2004) may, hence, in part be responsible for the r-strategy dominance in the Fucoid as well as Non-fucoid vegetation in the present study. The Fucoid vegetation in Krono¨ren not only displayed K-strategy dominance in the ABC curves, but had also greater faunal diversity in the 3 most sheltered sites (K1eK3) than did the Non-fucoid vegetation as well as distinct seperated from the Non-fucoid vegetation in terms of nMDS ordination. In contrast, the algal vegetation in Asko¨ did not display any differences in terms of ABC curves or Shannon index (H0 ) values, and was not as distinct in the nMDS plot as was the algal vegetation in Krono¨ren. Furthermore, the different types of algal vegetation in Asko¨ displayed a lower average dissimilarity of species contributions (51%) than did corresponding vegetation types in Krono¨ren (62%). As mentioned earlier, a major difference between Fucoid vegetation in Krono¨ren and in Asko¨ is in the biomass of filamentous algae: Fucus radicans in Krono¨ren are almost totally free of filamentous algae, whereas the Fucus vesiculosus in the nutrient-enriched Asko¨ area has a high load of filamentous algal biomass. This difference in the biomass of filamentous algae in the Fucoid vegetation may reflect the different degrees of eutrophication occurring in the 2 areas, the Bothnian Sea (Krono¨ren) not being affected by nutrient enrichment, unlike the Baltic Proper (Asko¨) (Ro¨nnberg and Bonsdorff, 2004). Thus, the greater diversity of faunal composition found in 3 of 5 investigated sites in the Fucoid compared to the Non-fucoid vegetation, as well as the K-strategy curve (shown for the fauna measurements), may indicate a diverse fucoid community not influenced by nutrient enrichment and eutrophication. However, differing nutrient levels are only one of the many parameters that differ between the investigated areas. Additional abiotic factors that may have an impact on the associated fauna in Krono¨ren and Asko¨ are depth, wave exposure, salinity and temperature; as well, there are the biotic factors, i.e., the different Fucus species themselves. One of the factors that thus also may have contributed to the greater dissimilarities between the Fucoid and Non-fucoid vegetation in Krono¨ren than in Asko¨ is the different sampling depths (4 m in Krono¨ren and 0.4 m in Asko¨). This, in turn, also resulted in different wave exposures (the Ez values for the sites in Krono¨ren were between 0.04 and 0.15, whereas the corresponding values for Asko¨ were 0.60e3.90). More sediments and organic matter accumulate along sheltered shores (Prathep et al., 2003) and at greater depths, and sediments are also more easily trapped in filamentous algae than in fucoids (Eriksson and Johansson, 2003). Since detritivores have been demonstrated to be positively correlated with sediment accumulation in algal turfs (Prathep et al., 2003), a greater abundance of deposit feeders and/or detritivores may be expected to be found in the Non-fucoid vegetation in Krono¨ren. In accordance with this hypothesis, deposit feeders like Macoma balthica and Chironomidae (Johnson, 1985), (even though the latter also may contain species that are herbivores
or predators (Cuker, 1983)) were more abundant in the Nonfucoid than in the Fucoid vegetation in Krono¨ren. Earlier field studies at Ask (Haage, 1975) have recorded sparse populations of M. balthica in Fucus vesiculosus vegetation, and the abundance correlated with F. vesiculosus stands that had a thick layer of detritus and sediment or were surrounded by softbottom environments. The greater differences between the 2 algal vegetation types in Krono¨ren than between the corresponding vegetation types in Asko¨ may indicate that the fucoid and filamentous algal vegetations in deeper parts of the littoral zone differ more in ecological function than do the same vegetation types in shallower parts. Thus, a shift from fucoid to filamentous algal vegetation would be expected to have a greater impact on faunal composition in deeper parts of the algal belt. Additionally, a shift is more likely to occur in deeper parts of the littoral zone, since the depth distribution of F. vesiculosus has declined due to reduced light availability (Kautsky et al., 1986), and studies have found that increased sediment deposition inhibits the recruitment success of F. vesiculosus (Berger et al., 2003; Eriksson and Johansson, 2003). It has also been found that F. vesiculosus may be positively affected by wave movement through the reduction of sediments and drift algae (Roos et al., 2004), an effect that is likely to decrease with depth. As Fucus radicans is not belt forming at depths less than 3e4 m in the northern Bothnian Sea, a shift in the depth extension of F. radicans in this area could eliminate the whole fucoid population. On the other hand, in the Baltic Sea, recolonization of the deeper parts of the F. vesiculosus belt, after a shift to filamentous algae, could be supported by shallowwater F. vesiculosus stands. 5. Concluding remarks This study has demonstrated that the small and lessinvestigated fucoid species Fucus radicans may be as important as the larger Fucus vesiculosus, since both Fucoid vegetation types harboured significantly greater faunal biomasses m2 in 3e4 of 5 investigated sites than did the corresponding Non-fucoid vegetation. These sites were in the lower range of wave exposure studied, indicating the Fucoid vegetations’ important role in sheltered coastal areas. Additionally, in the most sheltered sites, the diversity index for faunal communities in Krono¨ren was significantly higher in the Fucoid compared to the Non-fucoid vegetations. The faunal abundance did, however, not differ in any considerable way due to high number of fauna with low biomass associated with the load of filamentous algae. Furthermore, specific faunal species may also be negatively affected by a shift from fucoids to filamentous algae since, for example, a greater abundance of the sessile barnacle Balanus improvisus was found in the Fucoid vegetation in both areas. This species probably benefits from the fucoids’ broad fronds, which may also be important for the caddis fly Brachycentrus spp. This Trichoptera larva was only found in the Fucoid vegetation in Krono¨ren and its tubes were made entirely of pieces of F. radicans (pers. obs.). Furthermore, the abundances of, for example, Idotea baltica in the Asko¨ area and Gammarus spp. and Theodoxus fluviatilis
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in both investigated areas were 5 to 8 times higher in the Fucoid vegetation. Thus, we suggest that a shift from fucoids to filamentous algal vegetation may not only change the biodiversity and function of the associated invertebrates, but may also have an impact on fish species such as perch (Perca fluviatilis), a common species in coastal areas of the Baltic Sea (Nilsson et al., 2004), which is known to prey on these invertebrates (Mattila, 1992; Lappalainen et al., 2001). Acknowledgments We are especially grateful to Patrik Dinnetz for his advice on statistical matters. We would also like to thank Susanne Qvarfordt for her diving assistance, Stefan Lundberg at the Museum of Natural History of Stockholm for identification of the freshwater faunal species, Sofia Wikstro¨m and Lena Bergstro¨m for valuable comments on the manuscript and Patrik Kraufvelin for discussion of statistical and scientific matters. We also want to thank 3 anonymous referees for comments that greatly benefited this manuscript. The study was performed as part of the MARBIPP programme, financed by the Swedish Environmental Protection Agency and by the Stockholm and the Umea˚ Marine Research Centres. References Alley, R.B., Marotzke, J., Nordhaus, W.D., Overpeck, J.T., Peteet, D.M., Pielke, R.A., Pierrehumbert, R.T., Rhines, P.B., Stocker, T.F., Talley, L.D., Wallace, J.M., 2003. Abrupt climate change. Science 299, 2005e2010. Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P.S., Airoldi, L., Relini, G., Cinelli, F., 2001. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Marine Ecology Progress Series 214, 137e150. 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. Bergstro¨m, L., Tatarenkov, A., Johannesson, K., Jo¨nsson, R.B., Kautsky, L., 2005. Genetic and morphological identification of Fucus radicans sp. nov. (Fucales, Phaeophyceae) in the brackish Baltic Sea. Journal of Phycology 41, 1025e1038. Bonsdorff, E., Blomquist, E.A., Mattila, J., Norkko, A., 1997. Coastal eutrophication: causes, consequences and perspectives in the Archipelago areas of the northern Baltic Sea. Estuarine, Coastal and Shelf Science 44 (Suppl. A), 63e72. Bustamante, R.H., Branch, G.M., 1996. Large scale patterns and trophic structure of southern African rock shores: the roles of geographic variation and wave exposure. Journal of Biogeography 23, 339e351. Casatti, L., Langeani, F., Ferreira, C.P., 2006. Effects of physical habitat degradation on the stream fish assemblage structure in a pasture region. Environmental Management 38, 974e982. Clarke, K.R., Warwick, R.M., 1994. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory, Plymouth, UK, 144 pp. Cederwall, H., Elmgren, R., 1990. Biological effects of eutrophication in the Baltic Sea, particularly the coastal zone. Ambio 19, 109e112. Cuker, B.E., 1983. Competition and coexistence among the grazing snail Lymnaea, Chironomidae, and microcrustacea in an arctic epilithic lacustrine community. Ecology 64, 10e15. Dubois, S., Commito, J.A., Olivier, F., Retie`re, C., 2006. Effects of epibionts on Sabellaria alveolata (L.) biogenic reefs and their associated fauna in the Bay of Mont Saint-Michel. Estuarine, Coastal and Shelf Science 68, 635e646.
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