MOLLUSCA. Theodoxus fluviatilis (L.) Hydrobiidae. Limapontia capitata (O.F. Mtiller). Mytilus edulis L. Cerastoderma glaucum (Bruguire). Macoma balthica (L.).
In Coflaboratlon with the Netherlands Institute for Sea Research
ELSEVIER
Journal of Sea Research
37 (1997) 153-166
Community structure and spatial variation of benthic invertebrates associated with Zosteru marina (L.) beds in the northern Baltic Sea Christoffer Bostrijm, Erik Bonsdorff * HusB Biological Station and Department of Biology, Abe Akademi University, FIN-22220, Emkarby, Aland Islands, Finland Received
20 May 1996; revised version received 4 November
1996; accepted
25 November
1996
Abstract
The distribution and bed structure of eelgrass (Zosteru marina L.), and its importance for associated fauna1 communities in the coastal areas of the northern Baltic Sea are poorly known. The spatial distribution of the fauna associated with Zostera was studied at five localities in SW Finland in 1993-94. Zostera was common on all localities, but the beds varied in terms of area (1-5 m diameter), density (50-500 shoots/m*) and blade length (20-l 10 cm). A total of about 40 species or taxa were recorded. The zoobenthic infauna showed significant spatial differences, and total abundance and species diversity were significantly higher in the Zostera beds than in adjacent bare sand. The total abundance in Zostera ranged from 25 000 to 50 000 ind/m* and in sand from 2500 to 15 000 indIm*. The mean number of species in Zostera ranged from 5.9 to 8.8 spp (B = 1.76-2.54) and in sand from 2.2 to 5.5 spp (K = 1.67-2.31). The epifauna in Zostera was numerically dominated by grazing gastropods (Hydrobiidae) and copepods. The epifauna is an important community component, which contributes to the total diversity of the Zostera assemblage. These systems are among the most species-rich components of the shallow soft-bottom ecosystems in the northern Baltic Sea. The mechanisms structuring both the Zostera and the ambient sand-bottom habitats are presented. Keywords:
Zostera marina;
community structure; zoobenthos; epifauna; Baltic Sea
et al., 1993), and by altering predator-prey relation-
1. Introduction Vegetated sediments support higher densities of animals and higher species diversity than nearby
unvegetated sediments (Stoner, 1980; Pihl, 1986; Heck et al., 1989; Edgar et al., 1994). Beds of aquatic vegetation exert a strong influence on the spatial distribution of associated fauna by modifying the hydrodynamic environment (Fonseca and Fisher, 1986), stabilising the sediment (Orth, 1977), providing new habitats and substrates for epibiota (Neckles *Corresponding author. erik.bonsdorfWabo.fi
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ships due to increased habitat complexity (Nelson, 1979; Nelson and Bonsdorff, 1990; Mattila, 1995). The distribution of eelgrass Zusteru marina (L.) in the northern Baltic Sea (Archipelago Sea, SW Finland) has been poorly investigated since the 1950s (Luther, 195 la; Luther, 195 lb). Pioneering quantitative investigations of eelgrass communities in the Baltic Sea were carried out in Polish coastal waters (Bursa et al., 1939), while the first studies in the northern Baltic Sea, including both fauna and flora, were made in Sweden by Jansson (1969) and Gothberg and Rondell (1973). Quantitative fauna1 investigations of Zostera communities in Finland are
154
C. Bostriim, E. Bonsdo$/Journal
of Sea Research 37 (1997) 153-166
Fig 1. The investigated Zostera marina localities around the &and Islands (A-D) and in SW Finland (E) in the northern Baltic Sea (insert).
sparse, and have mainly been carried out in the Tv;irminne area (Fig. 1). at the shallow sandy southern coast of the Hango peninsula (Lappalainen, 1973; Lappalainen and Kangas, 1975; Lappalainen et al., 1977), though all shallow sandy bottoms with sufficient water circulation, salinity, and light regime are potential habitats for the species. These earlier Finnish studies aimed at describing the temporal patterns of the fauna (both seasonal and annual) in a single Zosteru community (Tvarminne). However, studies of the possible effects of Zosteru on the spatial distribution of the fauna are lacking, although Mattila (1995) compared the infauna of a Zostera community with that of bare sand in the Aland Archipelago. The only field study to date describing the composition of the epibenthic (associated strictly with the plants above the sediment surface) community of Zosteru beds in the northern Baltic Sea, was carried out in the Asko area (7-8%0 S) in 1969 (Gdthberg and Rondell, 1973), but no quantitative data on the epibenthic community from the less saline (5-6.5%0) Finnish archipelago waters exist. The present study aims at describing the ecological role of Zosteru (occurring in low abundance at the limit of its distribution) in regulating benthic community structure (both in- and epifauna) and describing the mechanisms structuring the Zusteru and sand habitats. The following questions were posed:
(1) are there detectable infaunal differences between vegetated (Zosteru meadows) and unvegetated areas (sandy bottoms), and (2) what is the importance of Zosteru on animal species composition abundance, distribution and diversity? Further, the composition of the epibenthic invertebrate community (fauna associated with the Zostera leaves above the sediment surface) was analysed and treated as a separate unit. 2. Study area 2.1. General characteristics The young (about 3000 years in its present brackish form), semi-enclosed, and non-tidal Baltic Sea shows a steeply decreasing salinity gradient from. the Kattegat in the south to the Gulfs of Bothnia and Finland in the north. In the northern Baltic Proper the surface water lies in the 5-lo%0 salinity range (Hallfors et al., 1981). The island-rich archipelagos of Aland and SW Finland are located between the Baltic Proper and the Bothnian Sea. The water temperature in the study area during the season (May-November 1993) ranged between 9-18°C (mean -13°C) and the salinity in, the area is ~6.5%0. Zostera marina, the only species of this genus recorded in the Baltic Sea, is the only truly marine phanerogam reaching these low-saline
C. Bostrtim, E. Bonsdofl/Joumal
coastal areas in the Baltic, and the inner border of the species lies at a mean salinity of 5%0 (Luther, 1951a,b; Lappalainen et al., 1977). In the Baltic Sea, Zosteru rely mainly upon vegetative reproduction for maintenance of existing beds, but flowering (Luther, 195 lb; Niemi, 1962) and fruit-bearing specimens (first findings in 1993) have also been reported (locality A; Bostrbm, 1995). The development of the vegetation and ecosystem structure is further controlled by the duration of the ice cover (4-5 months in the northern parts of the Baltic) (Hallfors et al., 1981) which (together with light intensity) has a strong influence on the depth zonation of the Zosteru belt, by producing a layer of low-saline water under the ice, which generally lasts from December to late April (Lappalainen et al., 1977). The benthic vegetation in the sub- and hydrolittoral is affected by a large seasonal amplitude in temperature (-0 to 20°C) during the short period of growth, while the increasing eutrophication of the Baltic (Jumppanen and Mattila, 1994) results in increased primary production and in subsequent degradation of annual filamentous macroalgae that form large drifting mats on the bottoms (Bonsdorff, 1992; Norkko and Bonsdorff, 1996a,b). 2.2. Localities investigated Zosteru beds at five localities were sampled in 1993-94 (Fig. 1): Four on the Aland Islands, namely Degersand (A), Appelo (B), Rankosklr (C) and Sando (D), and one on the Hango peninsula, SW Finland, Tvirminne (E). Locality E was also visited in order to study possible long-term changes (196893) in both the Zosteru vegetation and the associated fauna. The distribution of Zosteru at the localities was patchy, forming mosaic patterns with other phytobenthic species (e.g., Fucus vesiculosus L., Ruppia maritima L., Ruppia cirrhosa (Petagna) Grande and Potamogeton spp.), whereas homogenous and monospecific meadows could only be found at two localities (A and D). The localities were similar in depth (3-5 m), and semi-exposed to exposed with sand or sand/clay bottoms consisting mostly of medium-fine or fine sand sediment. The modal grain size in the Zostera sediment was smaller or similar (0.1254.5 mm) to the adjacent bare non-vegetated sand sediment (0.25-2.0 mm). The organic content
of Sea Research 37 (1997) 153-166
155
(loss of ignition, %) of the sediment reflected the stabilising effect of Zosteru, being higher (0.46-l .40%) in Zostera than in bare sand (0.3&0.57%; Table 1). 3. Material and methods Variations in fauna was studied at two spatial scales: (1) between bare and vegetated bottoms within localities (small scale; metres), and (2) between localities (large scale; 10-270 km apart) (Fig. 1). All sampling of infauna was done by SCUBA diving between 30 June and 2 September 1993. On each sampling occasion for infauna, 10 (Locality E: 11 sand and 12 Zosteru) replicate core samples (4.7 cm diameter, and 10 cm deep) were taken in dense Zostera and from adjacent unvegetated bare sand. The infaunal Zosteru and sand community at locality E was further sampled using a smaller corer (2.5 cm diameter, 10 samples in Zosteru, 10 in sand) in order to analyse the spatial distribution of newly settled (300-350 pm> larvae of Macoma balthica. An infaunal Zostera sample contained no other vegetation than the rhizomes. The Zostera invertebrate epifauna was investigated quantitatively at four localities, but only locality A was sampled intensively (n = 30) in August 1994 (n = 5-15 on the other localities, sampled 9 July to 2 September 1993, due to the descriptive nature of this study, and the labour-intensity of the sampling). Locality A had large (2-5 m diameter) and homogenous Zostera stands, and was thus considered most suitable for the sampling method. The design of the epifaunal sampler allowed simultaneous collection of Zostera blades and associated fauna. The epifauna was collected by pushing a plastic tube (10.3 cm diameter, height 25 cm, volume - 1250 cm3) covered with a 250 pm mesh vertically over the blades. Care was taken to keep the sampler off direct contact with the sediment. The vegetation was then clipped off by sliding a sharp metal plate into a slot situated 2 cm from the bottom of the sampler, thus sealing the tube, and preventing the material from slipping out. After a sample was enclosed, the sampler was taken to the surface, where animals and vegetation were carefully removed before transport to the laboratory. For analysis of the grain-size distribution in both vegetated and unvegetated habitats, one sediment
C. Bosrrtim, E. BonsdorJ/Joumal
156
Table 1 Physical characteristics, total abundance (J’) of the localities A-E Locality
Zostera
400-500 250-500 80-220 50-300 60-170
SE), number
37 (1997) 153-166
of species (spp/m2;
mean f SE), diversity
(H’), and evenness
Bare sand
cover
Shoots/m2
A B C D E
(ind/m2; mean i
of Sea Research
Org.
Gr.
(%I
(mm)
0.49 0.54 0.46 1.16 1.40
0.125 0.25 0.125 0.5 0.25
Spp.lm2
Abund./m2
32105 52682 23574 45 304 24994
f f f f f
3975 3849 2213 4288 3398
8.5 8.8 5.9 6.2 8.0
f0.3 f 0.7 + 0.5 f 0.6 i 0.7
H’
J’
2.54 1.83 1.76 1.85 2.40
0.64 0.47 0.51 0.50 0.62
Org.
Gr.
W)
(mm)
0.40 0.30 0.33 0.54 0.57
0.25 0.25 2.0 0.5 0.25
Abund./m2
Spp./m2
H’
J’
12853 16000 2594 14121 12632
5.5 5.4 2.2 4.6 5.3
2.31 1.70 1.67 1.84 2.12
0.67 0.57 0.59 0.58 0.59
f 2784 f 1527 f 678 f 1747 f 2200
f 0.6 LIZ0.3 k 0.4 + 0.5 + 0.4
Org.% = organic content of the sediment. Gr. = dominating grain size class.
sample (~1 kg sediment) was taken in each habitat. Sediment samples (n = 3-5) for the organic content were taken with a small corer (2.5 cm diameter). The Zosteru shoots were counted and measured (length) within a 50 x 50 cm frame (subdivided into four sections to facilitate counting) randomly thrown 5-15 times in each locality. No biomass estimates of Zusteru were made for this study. All samples of infauna were washed on a 500 pm mesh and then sorted alive (except for the core samples from locality D and the samples for newly settled M. balthica, which were preserved in a hexamine-buffered 4% formalin/seawater solution before sieving and sorting) using a dissecting microscope. The samples for newly settled M. bulthicu and the Zosteru epifauna were sieved on a 250 pm mesh in order to retain also the numerically abundant copepods. The Zosteru blades (mean sample size 6.5 g wwt/sample, range: 3-8.5 g) of the epifaunal samples were clipped into smaller pieces and placed in Petri dishes before sorting under a microscope, to ensure that all animals attached to the blade surfaces were counted. The zoobenthic production in terms of biomass was not included in this study. The samples for analysis of grain-size composition were dried for 24 h at 100°C before sieving through 11 sieve fractions (32, 16, 8, 4, 2, 1, 0.5, 0.25, 0.125, 0.074, 0.062 mm). Each fraction was then weighed separately. The organic content was measured as loss of ignition (ashing 3 h at 500°C) after drying for 24 h at 60°C. Differences in the spatial distribution of the zoobenthos (between the Zosteru and sand habitats, and between localities) were analysed by ANOVA
(Stat View 4.02@, @Abacus Concepts, Inc.), taking into account multiple comparisons by correcting the significance level according to the Bonferroni method, i.e., p -c 0.005 (= O.OS/lO). Diversity was measured by the Shannon-Wiener diversity (W) and its evenness component (1). The similarity between localities and the communities (Zosteru infauna, sand infauna, Zosteru epifauna) was measured using two indices, namely the Jaccard index (Rosenberg, 1977), based on species composition, and the Czekanowski coefficient (Bray and Curtis, 1957), based on both the number of species and their abundance. The relative variability of the epifaunal samples was compared by calculating the coefficient of variation, CV (SD divided by the mean). All values are given as mean f 1SE. 4. Results 4.1. Vegetation Zosteru marina was common on all localities, but the stands varied in terms of area (l-5 m diameter), shoot length (20-l 10 cm) and shoot density (SO-500 shoots/m*; Table 1). The largest and most homogeneous stands were found at localities A and D (2-5 m diameter). The mean blade length at all localities was about 50 cm, but smaller stands with blade lengths over 100 cm were found at locality A. At locality D two growth forms of Zosteru were observed: at 3 m depth shorter (20-30 cm) and dense (50-300 shoots/m*) stands than at 5 m depth, where slightly sparser (50-100 shoots/m*) stands with longer (80 cm) blades were observed.
C. Bostram, E. BonsdoQf”/Joumal of Sea Research 37 (1997) 153-166 Table 2 Statistical comparisons localities A-E
(one-way
ANOVA) of the total abundance
A
B
2
(a) and number of species (b) between the Zosrera and sand habitats at
C
Z
S
S
1.57
D
2
S
E
Z
s
Z
S
(a) Total abundance A B c D E
Z S Z S z S Z S Z S
**
NS NS
NS NS
**
tO.OOO1 0.4256
NS
0.0413
0.0057
0.799 1 0.1459
NS **
0.1405
0.0091
NS
0.6190
0.963 1
NS NS NS **
