Higher filtration rates of the mussel Mytilus edulis

Higher filtration rates of the mussel Mytilus edulis gives the species competitive advantage over the barnacle Balanus improvisus in the northern Baltic Sea
Jonne KOTTA^1,*, Helen ORAV¹, Ilppo VUORINEN^2
1Estonian Marine Institute, Marja 4d, 10617 Tallinn, Estonia

²Archipelago Research Institute, University of Turku, SF-20500 Turku, Finland

^*Corresponding author: tel: [phone]; fax: [phone]; e-mail: [e-mail]
Abstract
Blue mussels (Mytilus edulis L.) and barnacles (Balanus improvisus Darwin) are the most prevalent filter-feeders in the northern Baltic Sea. We estimated the seasonal variation in the feeding behaviour of the species at semi-natural conditions. Grazing rates were always lowest in winter. Large and medium-sized mussels had higher grazing rates in summer than in autumn whereas opposite was true for small mussels and barnacles. Above 10 mm length blue mussels become competitively superior over barnacles in terms of individual feeding rate. Although barnacles are considered much better colonisers of vacated substrate, the differences in food acquisition may be the reason why blue mussels dominate in the areas of low physical disturbance. Based on the biomass distribution the population level grazing pressure of blue mussels was highest in more exposed areas and lowest in more sheltered areas. During summer and autumn blue mussels were able to remove daily 10-13 % of phytoplankton stock in the outer archipelago, 4-6 % in the middle archipelago and less than 1 % in the inner archipelago. During winter these values were 2-3, 0.5-1 and less than 0.25 %, respectively.
Keywords: Barnacle; Biodeposition; Blue mussels; Clearance rate

Introduction

Blue mussels (Mytilus edulis L.) and barnacles (Balanus improvisus Darwin) are the most conspicuous filter feeders in the northern Baltic Sea. The species are most prevalent on hard bottoms above the halocline where, owing to low predation (Kautsky, 1995; Öst and Kilpi, 1997) and high input of nutrients (Wulff et al., 1994; Bonsdorff et al., 1997), they often form extensive multilayered mats (Segerstråle, 1957; Kautsky, 1981; Kautsky, 1995). At high densities the filter-feeders are capable to deplete phytoplankton in the water (Cloern, 1982; Fréchette and Bourget, 1985) and therefore be often food limited (Kautsky, 1981).

Space and food are considered the major factors determining the distribution of benthic organisms on the hard substrate in the northern Baltic (Kautsky, 1981). Recent investigation (Laihonen et al., 1997) has indicated that barnacles are superior over blue mussels in terms of settlement efficiency when the primary substrate is available. However, based on the field observations barnacles prevail only at highly disturbed environment whereas blue mussels dominate at much wider range of biotopes constituting more than 90% of the benthic animal biomass in the Baltic proper (Kautsky, 1981, Kautsky, 1995). This suggests that the former species is opportunistic occupying quickly newly vacated substrate. Blue mussels, in turn, are expected to be more efficient grazers and in longer run have a potential to outcompete the barnacles unless the community will not be physically destroyed (i.e. effect of ice or storm).

To test this hypothesis of feeding superiority of blue mussel we measured the grazing pressure of populations of blue mussel and barnacle on phytoplankton at semi-natural conditions during one year. A similar study has been previously carried out to estimate the seasonality in the biodeposit production of blue mussels (Kautsky and Evans, 1987). We have no knowledge of comparable experimental data about barnacles. In our experiments grazing pressure was estimated by quantifying the clearance rate of chlorophyll in the water (for barnacles and blue mussels) and biodeposit production in terms of chlorophyll (for blue mussels).
Material and Methods
Seasonal grazing pressure of blue mussels and barnacles was recorded in a small laboratory near the shore at Kirkkolahti Bay, Seili Island, Finland (Fig. 1). The experiments were conducted during three periods: 11.08-18.08.1998, 28.10-02.11.1998 and 20.03-27.03.1999.

Small boulders with blue mussels and barnacles were collected at exposed rocky bottoms of 1-5 m depth adjacent to the laboratory. Mussels were divided into 3 size classes (small 9-11 mm, medium 19-25 mm and large 30-31 mm) and hold in separate trays within a system of running seawater originating from the sampling point in the field one week prior to experiments. This allows us to neglect the effect of a cut byssus which may contribute to the reduction of filtration performance as much as 50 % (Visman, 1990).

The groups of individuals of blue mussels and barnacles were incubated in 3 sets of four (barnacles, small, medium and large sized mussels) 55 l flow-through tanks (Fig. 1). Dry biomasses of mussels and barnacles within the tanks ranged between 263-295 g m^-2 and 48-80 g m^-2, respectively. Three tanks consisting no experimental animals served as a control.

The animals were fed natural particles. Seawater was pumped directly from Kirkkolahti Bay to a head tank and then distributed to the experimental tanks by gravity. Flow rates in the tanks were kept at 250 ml min^-1. The water in the head and experimental tanks was slowly stirred by aeration. Samples taken from trays not containing mussels demonstrated no significant settlement of particles in head and control tanks (total chl a < 0.2 μg per tray). On each morning all water from the experimental tanks was exchanged to establish field phytoplankton densities and remove possible sedimented material.

In each 2 hours the biodeposits (i.e. faeces and pseudofaeces where present) were cleaned from the trays by careful pipetting. Additionally water samples were taken. Water was filtered through Whatman GF/F filters. Samples were extracted in 96 % ethanol overnight. Chlorophyll a (Chl a) measurements were read on fluorimeter before and after adding 3 drops of 1 N HCl in order to identify the content of phaeopigments (Pha). Total chlorophyll (Chl a eq) was calculated as follows: Chl a eq = Chl a + 1.52 × Pha.

Both biodeposit production and clearance rate was used to estimate grazing rate of blue mussels. Grazing rate of barnacles was calculated from clearance rate. The comparison between biodeposit production and clearance rate of blue mussel showed no significant loss of chlorophyll in the guts of mussels. The survivorship of the mussels and barnacles was 100 % during the experiments.

Besides grazing experiments, blue mussels were sampled at 9 sites in the Archipelago Sea (Fig. 1). Yläpää, Yläpää-Korkeasaari and Korkeasaari represent inner archipelago, Saunasaari, Lohm and St. Gunkobb middle archipelago and Storskär, Glasaskär and Långskär outer archipelago, respectively. All sites had similar bottom type (rock) and topography (at least 12 m depth at 50 m distance from the shore).

Three replicate frame samples (20  20 cm²) were taken randomly by the diver at 3, 6 and 9 m depth in all 9 sites. Samples were preserved in 4% buffered formaldehyde solution. Wet and dry weight (48h at 60 C) of mussels were determined to the nearest of 0.5 mg. Natural biomass of blue mussels varied between 1 and 1453 g dw m^-2 in the study area (see also Table 1). Based on the biomass values, potential grazing pressure of mussels on phytoplankton was estimated at different part of the Archipelago Sea. Water chlorophyll values were obtained from the Regional Environmental Centre of SW Finland. In the calculations we assumed the presence of complete vertical mixing in the water column. Data about the growth of blue mussels in the region was obtained from the literature (Antsulevich et al., 1999).

Results

Interspecific variation

In general, barnacles had higher grazing rates than blue mussels when expressed as the amount of filtered chlorophyll per time and dry weight of soft tissue (Fig. 3a). Here higher grazing rates may be considered as an artefact reflecting very big share of supporting shell material to the total body weight of barnacles (1:40) as compared that of blue mussels (1:10). Therefore, the values of individual grazing rates (Fig. 3b, Table 2) are more appropriate for the purpose of comparison. Based on these figures, barnacles may be ranked among small-sized mussels. Medium-sized and large mussels had in all cases higher grazing performance than barnacles.

Seasonal variation

Grazing behaviour of the blue mussels and barnacles were estimated during three seasons (Table 3). There was a significant difference in water temperature between different seasons. Chlorophyll concentrations were similar in summer and autumn. During winter chlorophyll concentrations had dropped considerably. Temperature was close to the freezing point.

There was a strong seasonal variation in feeding behaviour of blue mussels and barnacles. The magnitude of these changes was affected by the size of the mussels. Grazing was always lower in winter as compared to other seasons. Large and medium-sized mussels had higher grazing rates in summer as compared to autumn, whereas opposite was true for small mussels and barnacles.

Individual filtration rates (Fig. 3c) followed similar pattern as individual grazing rates. Owing to lower chlorophyll concentrations the winter values of filtration rates were relatively more marked.

Spatial variation
Grazing impact of blue mussels varied strongly in space and time (Fig. 4). During summer and autumn the mussels were potentially able to remove daily 10-13 % of phytoplankton stock in the outer archipelago, 4-6 % in the middle archipelago and less than 1 % in the inner archipelago. During winter these values were 2-3, 0.5-1 and less than 0.25 %, respectively. Grazing pressure was highest at 3 m depth and lowest at 9 m depth in the middle and outer archipelago whereas no clear spatial pattern was found in the inner archipelago.
Discussion
Artificial reef experiments have indicated that barnacles are the most effective colonisers of newly vacated substrate in the Archipelago Sea (Laihonen et al., 1997). However, the region is characterised by almost uniform blue mussel community between the depths of 3 and 12 m (Antsulevich et al., 1999 and this study). Barnacles and mussels may cohabitate in the shallower areas. Close to the surface typically only barnacles prevail.

We believe that this discrepancy between settlement efficiency and real distribution range of blue mussels and barnacles can be explained by the differences in grazing performance. Our experiments showed that in terms of individual feeding rate barnacles become competitively inferior when the length of mussels exceeds 10 mm. This size corresponds to the mussel age of 2-3 years in Kirkkolahti Bay (Fig. 5, Antsulevich et al., 1999).

Taking that into account, the succession of benthic communities could be described as follows. When bare rock surface becomes vacant it will be soon covered by a dense population of barnacles. Population density of blue mussels is relatively low at the earlier stages of succession. Due to the quicker growth and, possibly, the immigration from adjacent areas, the share of total biomass and surface exploited by mussels gradually increases. In 2-3 years the mussels are potentially capable to consume the major part of available phytoplankton and hence, gradually outcompete the barnacles. Besides, as the concentration of phytoplankton is depressed near the seabed with the presence of dense filter-feeder community (Fréchette and Bourget, 1985; Fréchette et al., 1989) the bigger size of mussels (i.e. higher feeding level) gives them another selective advantage over barnacles.

However, the population of barnacles can be never totally ousted due to the regular renewal of the substrate by ice or storms at the shallower depths. On the other hand a few barnacles are also able to thrive at the dense mussel beds of deeper areas by settling near the siphonal apertures of the mussel (Laihonen and Furman, 1986). The currents produced by the blue mussel siphons enhance the feeding abilities, growth and hence, the reproduction potential of barnacles.

Kautsky and Evans (1987) suggested that seasonality in water temperature, water turbulence and phytoplankton biomass results three different seasons of feeding behaviour for blue mussel in the northern Baltic. Low temperature hampers the feeding activity during January to May, the main productive season is from the end of May to mid-September. Due to high resuspension of refractory particles, the biodeposition rates are highest despite of a moderate filtration activity in September to December.

Our data is mostly consistent with their findings. However, we did not observe higher biodeposition rates of mussels in autumn season, except for smaller individuals (10 mm). Similarly, barnacles had higher (not significantly) grazing rates in autumn. Here higher biodeposition may be attributed to higher filtration rate as there was no significant difference in water chlorophyll concentrations between summer and autumn. It seems highly probable that higher grazing rates of smaller filter-feeders in autumn was triggered by favourable size structure of suspended particles, i.e. the proportion of smaller particles in autumn considerably exceeded the summer value. It is expected that smaller filter-feeders have higher retention efficiency of smaller particles than bigger filter-feeders.

Temperature seems to play the major role in creating seasonal differences in filtration rates of mussels and barnacles. Filtration rate decreases with the temperature being about half of the summer value in autumn and a quarter of that in winter. Previously there has been reported that blue mussels may actively ingest seston at low temperatures (Loo, 1992). Low filtration rates of blue mussels at lower temperatures have been interpreted as energy saving adjustment serving to reduce high costs of filter-feeder during winter season when concentration of food particles is low (Newell and Bayne, 1980). In this study we observed a linear relationship between temperature and feeding rate of mussels. Despite of constant food level, filtration performance between summer and autumn differed two times. These results support rather the hypothesis of Jørgenson et al. (1990) according to which lower pumping rates at lower temperatures are caused by the increasing viscosity of the water.

Due to the stability of population (Antsulevich et al., 1999) and uniform population densities the grazing pressure of blue mussels varied little over wide areas in the Archipelago Sea. The region may be divided into three distinguished parts: outer, middle and inner archipelago. More exposed is the region higher is the grazing pressure. The utilisation rate of phytoplankton by filter-feeders vary with benthic boundary-layer flow conditions (Fréchette et al., 1989). In outer archipelago stronger vertical mixing increases the amount of food available to the blue mussels and hence, support high biomasses. Extremely low values of population grazing in the inner archipelago may be attributed to the lower wave energy input to the system but as well as low salinity values.

Phytoplankton is able to renew daily 1-52 % of its stock depending on season and eutrophication level of the region (A. Jaanus pers. comm., Fig. 6). Grazing removal of phytoplankton by blue mussels is not sufficient to deplete the phytoplankton stock in the coastal areas of northern Baltic Sea. Its impact is highest at the shallower parts of the outer archipelago where the grazing may occasionally exceed the values of phytoplankton production (especially in autumn). However, the phytoplankton production is always higher than grazing in the deeper areas and therefore consumption never exceeds elimination in the coastal areas as a whole.
Conclusions
Blue mussels have higher individual grazing rates than barnacles when their length exceeds 10 mm. Grazing pressure of barnacles and blue mussels (i.e. nutrient flow to benthic system via biodeposits) decreases from summer to winter. Highest grazing effect was observed in the most exposed and lowest in the isolated areas. The population of blue mussels is able to deplete the phytoplankton stock in the overlying water only in limited areas.
Acknowledgements
This study was done at Seili Field Station, University of Turku and funded by EU BASYS project.
References
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Table 1. Average biomass of blue mussels with standard error values (s.e.) at different depths in 9 study sites of the Archipelago Sea

Area	3 m	6 m	9 m
1. Yläpää	89.8 (17.8)	74.7 (25.4)	153.4 (3.5)
2. Yläpää-Korkeakari	9.1 (4.4)	20.3 (2.2)	190.9 (44.5)
3. Korkeakari	18.5 (7.3)	115.3 (15.1)	83.3 (21.2)
4. Saunasaari	105.5 (34.6)	62.1 (12.0)	431.3 (34.0)
5. Lohm	589.7 (70.7)	827.4 (85.3)	465.9 (179.1)
6. St. Gunkobb	566.0 (81.5)	1.0 (0.6)	739.2 (117.9)
7. Storskär	1452.8 (185.9)	914.0 (51.8)	161.7 (65.8)
8. Glasaskär	1035.9 (182.8)	674.2 (202.0)	94.9 (9.8)
9. Långskär	1325.9 (191.5)	824.8 (86.3)	135.8 (26.6)

Table 2. Mean values of length (mm) and soft tissue dry weight (g) of barnacles (B), small (M*), medium-sized (M**) and large mussels (M***) at different seasons. Standard error values (s.e.) and the number of measurements (N) are indicated

Season	Group	Length	s.e.	Weight	s.e.	N
summer	B	7.3	0.2	0.00135	0.00030	69
	M*	10.4	0.2	0.00412	0.00021	213
	M**	22.3	0.3	0.01766	0.00075	172
	M***	30.8	0.4	0.04082	0.00110	42
autumn	B	6.0	0.2	0.00070	0.00002	320
	M*	9.1	0.2	0.00403	0.00043	111
	M**	24.9	0.3	0.04441	0.00122	91
	M***	31.2	0.5	0.05936	0.00169	54
winter	B	4.8	0.1	0.000075	0.000002	264
	M*	11.2	0.2	0.00894	0.00027	115
	M**	19.5	0.5	0.03152	0.00251	48
	M***	-	-	-	-	-

Table 3. Average water temperature (C) and total chlorophyll a concentration (μg l^-1) during different seasons

Season	Temperature	s.e.	Chlorophyll	s.e.
summer	16.17	0.27	3.25	0.07
autumn	7.63	0.14	3.89	0.31
spring	2.49	0.10	0.80	0.04

Figure 1. Study area.

Figure 2. Experimental cage.

Figure 3. Weight specific and individual grazing (A, B) and filtration (C) rates of barnacles and blue mussels during three seasons.

Figure 4. Potential removal of phytoplankton stock by the population of blue mussel at different depth levels in the different parts of the Archipelago Sea. The numbering of the study sites is same as in table 1.

Figure 5. Relationship between the length and age of blue mussel around the coastal sea of Seili Island (Antsulevich et al., 1999).

Figure 6. Potential removal of phytoplankton production by the population of blue mussel at different depth levels in the different parts of the Archipelago Sea. The numbering of the study sites is same as in table 1.