86 J
. Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
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
3.1. Field study 3.1.1. Algal fauna: community composition and abundances
˚
Our results show that drifting algal mats in the Aland archipelago at times can harbour high abundances of invertebrate macrofauna Table 1. Twenty-six taxa were found in
the algal mats and 20 taxa in the sediments Table 2. The numerically most abundant taxa in algal mats were Hydrobia spp., Chironomidae, Ostracoda and newly settled
larvae of Cerastoderma glaucum Table 1, Fig. 3. Other taxa such as Oligochaeta, Hydrachnidae and Gammarus spp. were present in 100, 85.5, and 74.7 of the samples
respectively, but never in high densities. The abundance of copepods and nematodes was not estimated, but they were present in 97.6 and 94.0 of the samples respectively.
3.1.2. Spatial variation of the algal fauna Univariate community variables number of species, abundance, biomass, diversity,
evenness of the faunal community of the drift algae differed significantly between sites Kruskal–Wallis H-test, P
, 0.05. Multiple comparison tests P , 0.05 showed that the number of species was significantly lower at site G than at sites A and B, and also at site
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
87 Table 1
Algal cover 1 5 0–25, 2 5 25–75, 3 5 75–100 cover and total number of species, mean abundance,
biomass, diversity and evenness for the algal fauna at different sites. For each site the three most abundant species and their share of the total abundance are given. For site A results from sampling occasion A2 are
presented, as this is closest in time to when the other sites were sampled Site
Algal Species
Abundance Biomass
Diversity Evenness
Most abundant Abund.
cover number
ind g dwt g wwt g dwt
H 9
J species
A 3
22 596
6164 1.52
60.90 2.47
60.25 0.68
60.05 Hydrobia spp.
71 C
. glaucum Ostracoda
B 2
21 719
6172 1.25
61.28 2.19
60.23 0.59
60.06 Ostracoda
84 C
. glaucum Hydrobia spp.
C 3
20 750
6267 2.83
61.46 2.29
60.32 0.59
60.06 Ostracoda
81 Hydrobia spp.
C . glaucum
D 2
20 604
6223 0.68
60.14 2.29
60.24 0.67
60.06 Ostracoda
79 Hydrobia spp.
C . glaucum
E 2
13 57
628 0.01
60.01 1.92
60.12 0.69
60.03 Chironomidae
82 C
. glaucum Hydrachnidae
F 2
16 330
680 0.08
60.04 2.28
60.10 0.72
60.06 Chironomidae
73 Ostracoda
Hydra sp. G
2 12
248 634
0.05 60.01
1.82 60.04
0.74 60.10
Chironomidae 93
Hydra sp. Oligochaeta
H 3
16 861
6314 0.23
60.06 1.71
60.25 0.49
60.07 Chironomidae
89 Ostracoda
Hydrachnidae I
1 13
54 645
0.06 60.06
1.86 60.41
0.75 60.09
Chironomidae 93
Ostracoda Oligochaeta
I than at sites A, B and C. Total abundance was significantly lower at site I than at sites B and H, and also at site E than at site H. Total biomass was significantly lower at site E
than at sites A, B and C, and at site I significantly lower than at sites A and C. The drift algae at sites A, B, C and H were thus the richest in terms of number of species, total
abundance and or total biomass Table 1. Though total abundance varied between sites, five taxa Hydrobia spp., C
. glaucum, Ostracoda, Chironomidae, Oligochaeta made up 86.2
610.1 of the total abundance at each site Fig. 3. Based on our observations, the state of algal decomposition seems to be a function of exposure to wind-wave
disturbance and depth. Sites E–I are relatively more exposed than sites A–D and the algae were generally more fragmented at these sites. Ostracoda and Hydrobia spp.
dominated at A–D, while Chironomidae dominated at E–I Fig. 3.
88 J
. Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104 Table 2
Taxa recorded in algae and in sediments, all sites and sampling occasions included 83 samples in total. For each species taxa it has been indicated whether they are infauna or epifauna, and their mean abundance in
algae ind g algal dwt has been given 1 indicates that the animals were not counted, only presence absence
noted. See Table 1 for relative abundances of the most abundant species at each site Species taxa
Algal Benthic
In epi Abundance
fauna fauna
fauna in algae
Bivalvia Macoma balthica L.
1 1
In 0.5
61.0 Mytilus edulis L.
1 Epi
3.4 66.7
Cerastoderma glaucum Bruguire 1
1 In epi
64.7 683.7
Gastropoda Hydrobia spp.
1 1
Epi 61.7
675.9 Theodoxus fluviatilis L.
1 Epi
0.9 62.4
Bithynia tentaculata L. 1
Epi 0.1
60.2 ¨
Limapontia capitata O. F. Muller 1
Epi 3.4
65.9 Crustacea
Ostracoda 1
1 Epi
139.2 6141.7
Copepoda 1
1 In epi
1 Gammarus spp.
1 Epi
7.1 613.6
Corophium volutator Pallas 1
1 In
0.1 60.2
¨ Bathyporeia pilosa Lindstrom
1 In epi
Iaera albifrons Leach coll. 1
1 Epi
1.2 62.2
Idotea baltica Pallas 1
Epi 1.6
63.6 Saduria entomon L.
1 In epi
Mysis mixta Liljeborg 1
Epi 1
¨ Polychaeta
Nereis diversicolor O. F. Muller 1
1 In
0.02 60.1
Pygospio elegans Claparede 1
1 In
0.03 60.2
Manayunkia aestuarina Bourne 1
1 In
0.1 60.4
Oligochaeta 1
1 In
22.4 619.9
Hirudinea Piscicola geometra L.
1 1
Epi 0.3
61.1 Insecta
Chironomidae 1
1 In epi
132.0 6156.8
Trichoptera 1
Epi 0.3
61.5 Arachnida
Hydrachnidae 1
1 In epi
15.8 618.6
Nematoda 1
1 In
1 Turbellaria
1 1
In epi 1
Nemertinea Prostoma obscurum Schultze
1 1
In epi 0.9
61.5 Hydrozoa
Hydra sp. 1
1 Epi
22.5 632.2
Correspondence analysis indicated that the four most sheltered sites i.e. sites A–D were very similar to each other but distinctly different from the remaining, more exposed
sites sites E–I. Sites E–I were also relatively more variable than sites A–D Fig. 4. Site G probably differs from all other sites because of some environmental factor we did
not measure, most likely sediment grain size, which is coarser at this site than at any of the other sites. The first two axes explained 65 of the variability. Canonical
correspondence analysis suggested site location i.e. longitude and latitude, exposure, algal condition and algal coverage to be important in influencing the algal fauna at
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
89
Fig. 3. Relative abundance of the five most dominant species at all sites. The degree of exposure to wind-wave disturbance at the sites has been indicated.
Fig. 4. Ordination diagram based on canonical correspondence analysis of the spatial variation of the algal fauna. The algal fauna at each site is represented by letters and the important environmental factors are
represented by arrows. The length and direction of the arrows correspond to the importance of the factor. Sites E–I are more exposed to wind-wave disturbance than sites A–D, and the algae are thus more fragmented at
sites E–I.
90 J
. Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
different sites, explaining 83 of the variability shown in Fig. 4 P 5 0.001. BIOENV
indicated that depth, exposure and algal cover were the most important factors influencing the algal fauna, explaining 49 r
5 0.7 of the variability in the algal fauna. To investigate the influence of benthic fauna on the composition of algal fauna at each
site, a correspondence analysis was carried out on raw data from the benthic samples using mean abundance values from each site, with sample scores from this analysis
included as environmental data in a canonical correspondence analysis with forward selection. This canonical correspondence analysis showed that the composition of
benthic fauna explained 18 of the variability in the algal fauna P
5 0.03 and that 63 of the variability in algal fauna was explained by a combination of composition of
benthic fauna, algal cover, algal condition and exposure. 3.1.3. Temporal changes in algal fauna
At site A drifting algal mats were sampled five times during 1996 sampling occasions A1–A5. Sampling began when algal mats first started appearing in July, and continued
until they began disintegrating in early October. Algal biomass peaked at A2 A3 and algal coverage varied between 50 and 100, decreasing towards the end of the sampling
period. The algae also became more fragmented over time.
No significant differences in number of species or total biomass were noted between sampling dates Kruskall–Wallis H-test, P
. 0.05, but multiple comparison tests showed that total abundance was significantly higher at A5 than at A1 P
, 0.01. In general, total abundance increased over time, whereas the average individual biomass
decreased Fig. 5. Correspondence analysis ordination indicated that the faunal community changed over time, with 59 of the variability explained by the first two
axes Fig. 6. Canonical correspondence analysis suggested date, algal cover and algal condition to be the most important factors influencing faunal composition over time, and
81 of the variability was explained by the first two canonical axes P
5 0.001. Fig. 6 indicates that, of the environmental variables measured, high algal biomass and cover
seem to be most influential at times A2–A4 time of maximum occurrences, whereas the condition of algae more fragmented influenced the fauna at A5.
Abundances for the six most important taxa at site A changed significantly over time Kruskal–Wallis H-test, P
, 0.05, followed by multiple comparison tests, P , 0.05, indicating that there are temporal differences in species utilising drift algae. Abundance
of Hydrobia spp. increased when juvenile mudsnails recruited to the algae towards the end of the summer A1: 121
650 →
A5: 255 6154 ind g dwt, although this increase was
not significant. At the same time the number of Ostracoda decreased when algae became more fragmented A1: 69
644 →
A5: 12 69 ind g dwt, being significantly higher at A1
and A2 than at A5. Abundance for Chironomidae peaked at A3 219 695 ind g dwt,
being significantly higher at A3 and A4 than at A1. Furthermore, abundances for the other important species decreased at A3. The number of C
. glaucum fluctuated throughout the sampling period, being significantly higher at A2 and A4 than at A1.
Limapontia capitata and Hydra sp. were recorded in the algae towards the end of summer and at A5 they became important, together constituting 33 of the total
abundance. The abundance of L . capitata was significantly higher at A5 than at A1 and
A2. The abundance of Hydra sp. was significantly higher at A5 than at A2, A3 and A4.
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
91
Fig. 5. Total abundance and the average individual biomass of the animals at different sampling occasions A1–A5; July–October at site A. Algal biomass peaked at A2 A3 and subsequently algal coverage decreased
and the algae became more fragmented.
During sorting of algal samples the condition of algae had been recorded, and the sites were subsequently grouped in to sites sampling occasions with Group I fresh algae B,
C, E, A1, A2, A3, A4 or with Group II more fragmented and degraded algae D, F, G, H, I, A5. Number of species and total biomass Mann–Whitney U-test, P
, 0.0001, as well as diversity P
5 0.0125 were significantly higher in fresh algae Table 3, whereas no significant differences were recorded with respect to abundance and evenness
P . 0.05. As Fig. 4 shows, also the multivariate analyses of different sites indicated
that algal condition influences the algal fauna. 3.1.4. Comparison of benthic and algal fauna
Generally, the algal fauna was dominated by Hydrobia spp., C . glaucum, Ostracoda
and Chironomidae Fig. 3, Table 1, whereas the benthic fauna was dominated by M .
balthica, Oligochaeta, Pygospio elegans, B . pilosa, as well as Hydrobia spp.,
Chironomidae and Ostracoda. In terms of functional groups, the algal fauna was dominated by surface detritivores whereas the benthic fauna was dominated by
suspension feeders surface detritivores and burrowing detritivores. For the benthic fauna no significant differences in number of species or evenness were detected between sites
Kruskall–Wallis H-test, P
. 0.05. Significant differences were found between sites for
92 J
. Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
Fig. 6. Ordination diagram based on canonical correspondence analysis of the temporal variation of the algal fauna at site A sampling occasions 1–5. The important environmental factors are represented by arrows. The
arrows for temperature and algal biomass overlap.
total abundance, biomass and diversity of the benthic fauna and multiple comparison tests P
, 0.05 showed that abundance was significantly higher at site F than at sites G and H, biomass was significantly lower at site G than at sites A and B, and diversity was
significantly higher at site B than at site F. In order to compare community parameters of algal and benthic fauna in general,
Table 3
a
Comparison of community parameters of algal fauna in fresh Group I and degraded Group II algae Species
Abundance Biomass
Diversity Evenness
per sample ind g dwt
g wwt g dwt H
9 J
Group I 15.0
62.9 575
6341 1.20
61.06 2.25
60.32 0.63
60.09 Group II
11.8 63.4
513 6337
0.28 60.26
2.04 60.39
0.66 60.14
P-value , 0.0001
0.5186 , 0.0001
0.0125 0.2324
N.S. N.S.
a
Number of species, total abundance, total biomass, diversity and evenness as mean x 6S.D. of all
sites samplings with fresh and all sites samplings with degraded algae, and statistical differences Mann– Whitney U-test between these two. Levels of significance given as P
, 0.001, P , 0.05 and N.S. not significant.
J . Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
93 Table 4
a
Comparison of community parameters of algal fauna and benthic fauna Species
Abundance Biomass
Diversity Evenness
per sample ind core
g wwt core H
9 J
Algal fauna 12.3
63.9 82.9
655.4 0.095
60.139 2.08
60.36 0.66
60.11 Benthic fauna
5.9 61.6
34.4 627.6
0.159 60.269
1.58 60.54
0.72 60.19
P-value , 0.0001
0.0001 0.5156
, 0.0001 0.0526
N.S. N.S.
a
Number of species, total abundance, total biomass, diversity and evenness as mean x 6S.D. of all benthic
and all corresponding algal samples, and statistical differences Mann–Whitney U-test between these two. Levels of significance given as P
, 0.001 and N.S. not significant, P . 0.05.
mean values of all benthic samples were compared with mean values of corresponding algal samples Table 4. Number of species, total abundance, and diversity were
significantly higher in the algae Mann–Whitney U-test, P 0.001. Similarity between
algal and benthic fauna was only 20 PRIMER; Bray–Curtis similarity index, mean abundance values, and a correspondence analysis performed on algal and benthic
samples mean abundance values plotted algal fauna and benthic fauna from different sites in two loose clusters with no overlap Fig. 7. The faunal community of drifting
Fig. 7. Correspondence analysis ordination of algal fauna 1 and benthic fauna 2 at different sites mean abundance values.
94 J
. Norkko et al. J. Exp. Mar. Biol. Ecol. 248 2000 79 –104
algae thus differs significantly from the resident benthic community of shallow sandy soft bottoms in the northern Baltic Sea.
3.2. Laboratory experiment 3.2.1. Aquaria conditions
During the experiments water temperature was 19.0 61.18C, salinity 5.760.1‰ and
pH 7.90 60.02 above the algae and in the controls. Oxygen saturation decreased rapidly
at the sediment surface under the algae, reaching hypoxic conditions only 6–12 h after addition of algae Fig. 8. In the algae oxygen saturation decreased to intermediate levels
35–75 O ; Fig. 8, and fluctuated depending on the structure and density of the algal
2
mat. At the termination of the experiments the water under the algae was anoxic and there was a strong smell of H S in more than half of the algal replicates. At the same
2
time oxygen saturation above algae was consistent at 100. 3.2.2. Survival and migration of test organisms in algae
Survival was good in all control treatments in all experiments Fig. 9 and the animals remained buried in the sediment. Survival was significantly lower Mann–Whitney
U-test in algal treatments than in controls for the 5 mm M . balthica P
5 0.0367 and for B
. pilosa P 5 0.0090. The position of the animals was recorded at the termination
of the experiments Fig. 9, and together with survival data, these results were used as a measure of a species ability to move up into a drifting algal mat. In all experiments, the
vast majority of all the animals 83 615 had emerged from the sediment in the algal
treatment, indicating that algae stress infauna and induce an escape response. The majority of M
. balthica both size classes emerged on to the sediment surface, but only a few moved into the algae, and none moved any higher than the first algal
layer. M . balthica 10 mm showed 100 survival in the algal treatment, indicating a
higher tolerance to hypoxia and H S compared to juvenile M . balthica 5 mm,
2
58.0 625.9 survival. Hydrobia spp. showed high survival 98.461.7 and mobility
in algae, and most of the mudsnails were found in the second and third algal layers, where oxygen concentrations were higher. Survival of N
. diversicolor was high 92.0
611.0, and these polychaetes seemed to move freely in the algae, showing no preference for any particular layer. Survival of B
. pilosa was low 30.0 612.7, and the
few surviving individuals were found in the upper algal layers Fig. 9.
4. Discussion