J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
81
¨ 10–15 years Makinen and Aulio, 1986; Kautsky, 1991; Bonsdorff et al. 1997. When
these algae are detached from their substratum they are transported to the sublittoral and deposited on relatively shallow
, 15 m soft bottoms as increasing amounts of drifting algae, covering ever increasing areas in late summer Olafsson, 1988; Bonsdorff, 1992;
Norkko, 1997. Drift algae occur both as small patches and as large homogenous mats, at times covering up to several hectares Norkko and Bonsdorff, 1996b. Small amounts
of drifting algae have always been present in this region, but the amounts recorded in recent years in the archipelago area are a new, eutrophication induced phenomenon. The
effects of the algae are therefore changing from stochastic to more predictable, and the algae have the potential to significantly alter the structure and function of this benthic
system Norkko, 1997.
No spatial and or temporal studies of species composition and abundance of the macrofauna associated with benthic drift algal mats have been conducted in the Baltic
Sea. The aim of this study was therefore to describe and quantify the invertebrate
˚
macrofauna occurring in benthic drift algal mats in the archipelago of the Aland Islands, northern Baltic Sea. We also experimentally tested differences in response to algal mats
in species representing different functional and taxonomic groups. We wanted thus to investigate the potential value of benthic drift algal mats as habitat for benthic fauna.
This was accomplished through sampling of algal mats in the field and through a series of laboratory experiments.
2. Methods
2.1. Field study 2.1.1. Study area
The field study was conducted in the western and northwestern parts of the outer
˚
archipelago of the Aland Islands, northern Baltic Sea 60 8N, 208E, Fig. 1. Nine sites
A–I were chosen on shallow 2–9 m sandy bottoms, with exposure to wind-wave disturbance varying from semiexposed to exposed. Oxygen saturation near the bottom is
usually high at these sites, but local hypoxia and anoxia have been recorded in connection with extensive occurrences of drifting algal mats Bonsdorff, 1992. Salinity
varies between 5.5 and 6.2‰. The benthic fauna has been extensively studied in this area see Bonsdorff and Blomqvist, 1993, for a review. At site A the effects of drifting
algal mats on infauna have been thoroughly investigated Bonsdorff, 1992; Norkko and Bonsdorff, 1996a,b; Norkko, 1997 and at sites B, F and H the invertebrate fauna
¨ associated with Zostera marina meadows has been studied Mattila, 1995; Bostrom and
Bonsdorff, 1997.
˚
Biomasses of drifting algal mats recorded in the Aland Island archipelago during 1990–1997 July–August, the time of maximum occurrences ranged from 50 to 830 g
2 2
dryweight dwt per m , with average values of approximately 220 g dwt per m ¨
Bonsdorff, 1992; Norkko and Bonsdorff, 1996a; Holmstrom, 1998. These drifting algal mats commonly range in thickness from 1 to 3 cm up to 20 cm and they consist mainly
of filamentous, ephemeral brown algae, e.g., Ectocarpus siliculosus Dillwyn Lyngb,
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Fig. 1. Map of the study area in the northern Baltic Sea 60 8N, 208E, with study sites A–I.
Pilayella littoralis L. Kjellman and Dictyosiphon foeniculaceus Hudson Grev. ¨
. 95 of the biomass, Norkko and Bonsdorff, 1996a; Holmstrom, 1998. 2.1.2. Field methods
This study was conducted in 1996 and all study sites Fig. 1 were sampled once for algal fauna between 3rd. July and 19th. August, after drifting algal mats started
appearing in July. The sites were also visited several times during May and June, but during this time no drift algae were observed, and it is therefore likely that the drift algae
had not been present at the sites for more than 1–3 weeks before they were sampled. For comparisons of algal fauna over time, site A was sampled a total of five times during
July–October i.e. on 27 7, 13 8, 23 8, 2 9, 3 10, sampling occasions A1–A5, respectively. A2 was used in the comparisons with other sites, which were sampled
only once, as this was closest in time. All sampling was done by SCUBA diving and all samples were obtained haphazardly along the bottom. To clearly distinguish between
algal and sediment dwelling fauna, and to avoid sampling fauna occurring at the sediment surface, the algal samples were collected by pulling an open-ended cylinder
diameter 10.0 cm, height 20.0 cm horizontally through the algal mat. A nylon stocking mesh size 0.1–0.5 mm was fitted over the end of the cylinder, and after the algal
sample [ | 5 g algal wetweight wwt] was inside the cylinder the nylon stocking was pulled forward until it enclosed the entire cylinder and then secured. No animals were
observed swimming away from the algal mats during sampling. Five to six replicate samples were taken at each site and the samples were taken 2–5 m apart. A separate
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
83
cylinder was used for each sample and the cylinders were transported to the laboratory in seawater. In the laboratory the algal samples were flushed out of the cylinders and
preserved in 4 hexamine [hexamethylenetetramine; CH N ]-buffered formalin.
2 6 4
Sieving the samples is not practical in the case of filamentous algae as the animals easily get trapped in the algae. The algae were sorted under a dissection microscope at 15
3 magnification and species composition, abundance and biomass wwt of the algal
macrofauna were recorded. Presence of meiofaunal taxa such as Nematoda, Copepoda and Turbellaria was noted. Also for each sample, the dominant algal species and state of
decomposition condition of the algae were noted, and their dwt estimated 24 h at 60
8C. The results are subsequently reported as abundance or biomass per g algal dwt. Number of species is given per replicate sample.
As drifting algal mats occur on shallow sandy soft bottoms, we wanted to compare the algal fauna with the resident benthic fauna of these sediments. Five to six replicate
2
benthic core samples diameter 4.7 cm, area sampled 17.3 cm , depth 10 cm were obtained from seven of the sites excluding sites C and E at the same time as the algal
samples. The benthic samples were obtained from bare sand at least 10 m away from the nearest algal mat. Samples were preserved in 4 hexamine-buffered formalin, washed
on a 0.5 mm mesh sieve and sorted under a dissection microscope at 15
3 magnifica- tion, and analysed as for the algal fauna. Results for the benthic fauna, including number
of species, abundance and biomass, are given per core sample. On each sampling occasion the algal coverage of the sea-floor at each study site was
estimated visually by diving over the site. Algal coverage was then allocated to one of three categories 1
5 small patches, , 25 coverage; 2 5 large patches, 25–75 coverage; 3
5 75–100 coverage. On shallow sandy bottoms drift algae can cover large areas; Norkko and Bonsdorff 1996a,b estimated the drift algae to cover an area of
¨ 2 hectares at site A for a 6 week period in July–August and Holmstrom 1998 reported
maximum occurrences of drift algae in August, with algae covering 80 of the sandy bottom at site A.
To facilitate comparison with benthic fauna, abundance of algal fauna was related to the areal coverage of algal mat by estimating the biomass of algal mats. On nine
different sampling occasions a core diameter 18.9 cm was pushed vertically through the algal mat into the sediment and dry weight of the algae was measured 24 h at 60
8C. To convert abundances and biomasses of the algal fauna to areal units for comparisons
2
with the benthic fauna a conversion factor of 100 g algae per m was used and then related to the area of the benthic core used. This value was chosen as a conservative
value, as it is close to the lower limit of the standard deviation of the actual values
2
recorded 181 6104 g dwt m .
2.2. Laboratory experiments 2.2.1. Test organisms
To test the ability of different species to move up into and survive in a drifting algal mat a series of five laboratory experiments were conducted. Based on previous studies
and data from the field sampling, we conducted experiments with four different species, all of which are important on shallow sandy bottoms, where drift algae may occur. The
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invertebrates studied represent different functional groups Bonsdorff and Blomqvist, 1993; Bonsdorff and Pearson, 1999.
The bivalve Macoma balthica L. is an important species in the Baltic Sea
˚ Segerstrale, 1962; Bonsdorff et al., 1995. It is classified as a semimobile suspension
feeder surface detritivore Bonsdorff and Blomqvist, 1993 and is tolerant to hypoxia Dries and Theede, 1974. M
. balthica has pelagic larvae and settling coincides both
˚
temporally and spatially with mass occurrences of drifting algal mats in the Aland archipelago Bonsdorff et al., 1995. Two size classes 3–5 mm and 10–15 mm of M
. balthica were used in the experiments. The mudsnails Hydrobia spp. are common on
sandy as well as hard bottoms and they also live associated with vegetation. These mudsnails are very mobile, feed mainly on detritus, and are continuously moving to
fresh patches of food. They are classified as mobile surface detritivores. Shell length of
¨ Hydrobia used in the experiments was 3–4 mm. Nereis diversicolor O. F. Muller is a
˚
polychaete common on shallow soft bottoms in the Aland archipelago. It is mobile, omnivorous, eating small invertebrates, algae and detritus, and can function as predator,
¨ surface detritivore, and suspension feeder Ronn et al., 1988; Nielsen et al., 1995. N
. diversicolor is tolerant to hypoxia, anoxia, and even hydrogen sulphide Vismann,
1990, and is commonly found under algal mats Norkko and Bonsdorff, 1996b. Length of N
. diversicolor used in the experiments was 40–50 mm. The amphipod Bathyporeia
˚ ¨
pilosa Lindstrom is common on exposed sandy bottoms in the Aland archipelago. It swims actively at night and is tolerant to short-term hypoxia Mettam, 1989; Sandberg,
1994. B . pilosa feeds on benthic diatoms and detritus, and it is classified as a mobile
carnivore surface detritivore. Length of B . pilosa used in the experiments was 3–5 mm.
2.2.2. Experimental set-up Drift algae for the laboratory experiments were collected from site B Fig. 1 1 day
prior to the start of each experiment. The algae, consisting mainly of the brown algae E .
siliculosus, P . littoralis, and D. foeniculaceus, were rinsed in running fresh water to
remove larger macrofauna and then checked to ensure the rinsing was successful. M .
balthica and N . diversicolor were collected from site B and B. pilosa from site H using
an Ekman–Birge grab and Hydrobia spp. were obtained from algae collected at site B. The aquaria for the laboratory experiments were 50 cm high
3 9.1 cm diameter plexiglass cylinders volume 3.25 l, Fig. 2. Each aquaria had a 5 cm layer of air-dried
and sieved mesh size 0.5 mm sand as sediment. Each species was tested separately and the five experiments were conducted using: 1 ten M
. balthica 5 mm size class; 2 five M
. balthica 10 mm size class; 3 50 Hydrobia spp.; 4 five N. diversicolor; and 5 20 B
. pilosa in the replicate aquaria. The number of animals in the experimental aquaria corresponded to densities recorded in the field. The animals were acclimatised
for 24 h before the experiments were started by adding the algae. To the algal treatment
2
five replicates a total 13.0 g wwt algae corresponding to 2000 g wwt m or 400 g
2
dwt m was added in three layers separated by a thin net mesh size 1–2 cm. Each
2
layer was approximately 4 cm thick Fig. 2. Four-hundred g dwt m algae was chosen as this corresponds to the amount of algae used by Norkko and Bonsdorff 1996a,b,c in
laboratory and field experiments. No algae or nets were added to the control treatment five replicates.
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
85
Fig. 2. Schematic detail of experimental aquarium; algal treatment. Diameter of cylinder 9.1 cm and actual height of cylinder 50 cm, thickness of each algal layer 4 cm.
The aquaria were covered with black plastic to the height of the algae in order to simulate light conditions prevailing under a more extensive algal mat. In control
treatments the aquaria were covered only to the height of the sediment surface. Both algal treatments and controls were aerated and oxygen saturation above, in and under the
algae was measured before the addition of algae, and then again after 12, 24, 48 and 72 h, using Winkler titration. Water samples in and under algae were obtained using a
syringe to pierce silicon filled holes in the walls of the aquaria Fig. 2. The experiments were conducted over 72 h with a 12:12 h light dark period. When the experiments were
terminated, the algal layers were retrieved separately, and survival and position in sediment, on sediment or in any of the three layers of algae of the animals were
recorded.
2.3. Data analysis 2.3.1. Univariate
As the analysis of the algal fauna revealed a nonnormal distribution Shapiro–Wilk W-test, differences in algal fauna between sites and between sampling occasions site A
were investigated using the nonparametric Kruskal–Wallis H-test Sokal and Rohlf, 1981. Multiple comparisons between sites and between sampling occasions were then
performed using a formula described in Zar 1984. The benthic fauna was analysed in the same way. The Shannon–Wiener diversity index H
9, log base 2 and its evenness
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component J were calculated for all replicate algal and benthic samples. For comparisons of algal and benthic fauna and for statistical analysis of data from the
laboratory experiments the Mann–Whitney U-test was used. All values are given as mean
6standard deviation x6S.D.. 2.3.2. Multivariate
To describe temporal and spatial patterns in the invertebrate community of the drift algae, abundance data was analysed using correspondence analysis CANOCO; ter
Braak, 1988 and using the Bray–Curtis similarity index followed by nonmetric multidimensional scaling MDS ordination Kruskal and Wish, 1978; PRIMER; Clarke
and Warwick, 1994. Analyses were carried out on raw and transformed data presence absence, fourth root transformation, but only solutions using raw data are presented
here, as we were interested in differences in abundances as well as species composition. Correspondence analysis and MDS ordinations gave very similar results and therefore
only the correspondence analysis ordination plots are presented here. Canonical correspondence analysis ter Braak, 1988 and BIOENV Clarke and Ainsworth, 1993
were used to examine relationships between structure of faunal communities and environmental data. Again analyses carried out on raw data are presented. Environmen-
tal parameters used in canonical correspondence and BIOENV analyses included time date, depth, algal biomass, algal coverage, algal condition, exposure to wind-wave
disturbance, and longitude and latitude of the sites. In addition, correspondence analysis scores for ambient benthic fauna at each site were used as an environmental factor in a
canonical correspondence analysis, in order to investigate the influence of the structure of benthic fauna on the structure of algal fauna.
3. Results
