­Blue mussel (Mytilus spp.) cultivation in mesohaline eutrophied inner coastal waters: mitigation potential, threats and cost effectiveness

Study site

The coast of the federal state Mecklenburg-Vorpommern is characterized by several bays, backwaters (Haffe), estuaries and lagoons embedded by islands and peninsulas that form the inner coastal waters (Fig. 1). Salinity classifies two types of inner coastal waters for the German Baltic coast: oligohaline (0.5 to 5–6 PSU) and mesohaline inner coastal waters (5–6 to 18–20 PSU) (Schernewski et al., 2004).

Wismar Bay and Salzhaff in the west are both part of the Bay of Mecklenburg with an intense water exchange with the open Baltic Sea (Schlungbaum & Baudler, 2001).

The Warnow Estuary, surrounded by the city of Rostock, is the transition zone between the river Warnow and the Baltic Sea. Salinity levels in the Warnow Estuary are strongly influenced by stratification caused by river water and Baltic water inflow.

The Barther Bodden is part of the Darß-Zingst Bodden chain. Its salinity level is indirectly influenced by water exchange from the open Baltic Sea and the oligohaline Bodstedter and Saaler Bodden (Schumann et al., 2006). The Strelasund is a strait that separates the Island of Rügen from the German mainland. The Westrügensche Bodden, Greifswalder Bodden (GWB), Kleiner Jasmunder Bodden, and Nordrügensche Bodden all form the coastal lagoons around the Island of Rügen. Salinity levels of coastal lagoons vary according to direct or indirect water exchange with the Baltic Sea (Fig. 1, Table 1).

The GWB is the biggest inshore basin located in north east Germany, limited by the mainland to the south and the Island of Rügen to the West. The average water depth is 5.8 m, with a maximum depth of 13.6 m. Sediment types consist mostly of mud, sand, and clay gravel-mixture. Based on the lack of hard substrate (Kanstinger et al., 2018), only a limiting and or fluctuating) Mytilus spp. stock can be expected. It is most likely that mussel larvae enter GWB from mussel beds outside, which can be found on reef structures around Rügen Island (Darr, Gogina & Zettler, 2014). Salinity levels range from 6–8 PSU. Water temperatures are highly influenced by seasonal atmospheric temperature regimes.

The GWB plays an important role, both ecologically and economically. While tourism and coastal fishing are essential for local employment (Obenaus & Köhn, 2002; http://www.statistik-mv.de), the GWB serves also as an important spawning ground of the herring stock in the western Baltic Sea (Kanstinger et al., 2018). High nutrient inputs in the past have led to heavy eutrophication (Munkes, 2005). As a result, submersed macrophyte cover declined from 90% to 15% and the GWB turned into a phytoplankton-dominated ecosystem (Munkes, 2005). Altogether, it seems that present mitigation measures in the catchment area are not sufficient to return to a GES and supporting internal measures are needed.

Hydro-chemical and biological data analysis

The hydro-chemical and biological data were provided by the State Agency for Environment, Nature Conservation and Geology Mecklenburg-Vorpommern (LUNG). Monitoring stations provide monthly data for total nitrogen (TN) and phosphorus (TP), dissolved inorganic nitrogen and phosphorus, Chl. a concentration, and Secchi-depth for the period from 1990-2018. Dissolved inorganic nitrogen (DIN) is the sum of nitrate, nitrite, and ammonium. Samples for dissolved nutrients were stored dark until filtration through cellulose-acetate filters (pore size 0.45 µm) followed by freezing. Dissolved inorganic phosphorus (DIP) was determined as soluble reactive phosphorus by using the molybdenum blue method (Strickland & Parsons, 1972). The percentage share of non-bioavailable DIP was not determined. TP and TN were digested in a microwave with peroxodisulfate (DIN11905-1 1998). Total and dissolved nutrients were measured in a continuous flow analyser (Skalar Inc., later Alliance Instruments (Malcolm-Lawes & Wong, 1990; DIN13395 1996; DIN11905- 1 1998; DIN11732 2005). Chl. a was determined fluorometrically (665 nm) after filtration (GF/F, 0.7 µm), extraction with ethanol, and acidification (ISO 10260:19922).

To evaluate whether internal mitigation measures are suitable, time series analysis of total nutrients (TN & TP), Chl. a concentration, and Secchi depth were conducted for the period between 1990 and 2018. The data was split into three periods and average annual concentrations from 1990–1999, 2000–2009, and 2010-2018 were compared. The time series were analyzed using the Mann-Kendall test to identify whether the measured values of the time series are randomly distributed or if trends occur in the data. The level of significance was set to 0.05. Afterwards, values were compared with new WFD target concentrations (Schernewski et al., 2015).

A general approach to managing eutrophication is the control of nutrient loads (N, P) essential for primary production. It has to be known weather phytoplankton biomass responds to changes in nitrogen or phosphorous in the water column. To investigate this, monthly DIN/DIP ratios and Chl. a concentration for all water bodies were compared. Simple linear regression was used to describe the monthly relationship between TN or TP to Chl. a concentration. To investigate how nutrient reduction potentially improves water transparency, simple linear regression models were used as well. Data was ln-transformed when necessary.

Pilot blue mussel farms setup

Pilot farm 1 is located in the Hagensche Wiek, a bay in the north eastern part of GWB (Fig. 1). The cultivation unit consisted of five parallel longlines (Fig. 2). Each longline moored in a depth between 5.0 and 6.0 m using dead weight anchors of 250 kg. Every longline was attached with 50 m collector material, consisting of one mm thick and 50 mm wide polypropylene bands reaching up to 3.5 m water depth. Pilot farm 1 was deployed in April 2017 and was operated until October 2019. During the operating period, the collector material was used for spat collection and mussel grow out.

A smaller test farm (pilot farm 2) was located in the Wieker Bay (WB) (Fig. 1). The setup consists only of two longlines, each 10 m long (Fig. 2). The collector band material matches the one of pilot farm 1 and the loops extended from 1 m to 1,5 m. Pilot farm 2 was deployed in June 2017.

Field and laboratory experiments

Mesocosm experiments were carried out at GWB and WB to estimate the individual clearance rate at high Chl. a concentrations of Mytilus spp. The reduction of Chl. a was measured using an in vivo fluorometer (Algae Torch, bbe-Moldaenke, Germany).

Additional laboratory experiments tested different Chl. a concentrations and their effect on the clearance rate (CR) of Mytilus spp. During the laboratory experiments, different concentrations of Rhodomonas spp. were added to a well-mixed and aerated aquarium with defined volume of artificial seawater and a group of mussels (n = 20). The reduction of Chl. a concentration was measured using a handheld fluorometer (AquaFluor, Turner Designs, USA). The clearance rate was determined by the exponential decrease in Chl. a concentration as a function of time using the equation CI = a*(V/n), where V = volume of water, n = number of filtering mussels, and a = slope of the regression line in a semi-ln plot of the reduction of Chl. a. Measurements were repeated three times. Control runs without mussels were conducted to evaluate possible sedimentation. Mesocosm and laboratory experiments were conducted at water temperatures of 20 °C.

Nutrient harvest yields were estimated by the nitrogen and phosphorus content of cultivated blue mussels. Mussel tissue and shells of all individuals were pooled, freeze- dried, and ground prior to analyzing carbon and nitrogen with an auto-analyzer (Elementaranalysator EA 3000). Phosphorous was determined in mussel ash using an alkaline persulfate oxidation after Hansen & Koroleff (1999).

The bio deposition of faeces and pseudo-faeces was measured with sediment traps. The traps were deployed within the GWB farm and at a reference point 100 m SW (N54°18,839; E13°40,728) in May 2018. Additionally, sediment traps were deployed at a commercial mussel farm (Farm size = 1 ha) in the Kiel Fjord. Trap contents, including all suspended particles, were filtered onto Whatman GF/F filters, dried, and weighed. Total organic content (TOC) was measured as loss on ignition. Furthermore, sediment samples were taken within GWB farm and the reference point. Subsequently, TOC was measured as loss on ignition of dry matter.

To measure the Vibrio spp. abundance within the pilot mussel farm in GWB and the reference location, samples were taken of surface water, sediments, sediment traps and mussels.

The total number of Vibrio spp. from water samples was determined by filtering water volumes of 10 and 50 mL through 0.45 μm-pore-size mixed cellulose ester filters (MontaMil^® Membrane Filters, Frisenette ApS, Knebel, DK). All filters were placed onto thiosulphate-citrate-bilesalts-sucrose agar plates (TCBS agar) (SIGMA-ALDRICH, Missouri, US1A) and incubated for 24 h at 37  °C. Sediment and sediment trap samples were serially diluted and plated on TCBS agar. Fresh mussel samples collected at the mussel farm were transported in cooling boxes and processed within 8 h of collection. Sample preparation and homogenization was done according to the CEFAS Standard Operating Procedure—Detection of Vibrio parahaemolyticus in Bivalve Molluscan Shellfish (http://www.crlcefas.org). Serially diluted sample homogenate was plated on TCBS agar. After 24 h of incubation, colonies were counted and the number of total Vibrio determined as colony forming unit (CFU) 100 mL⁻¹ for water, CFU 100 g⁻¹ for sediment samples and CFU g⁻¹ mussel tissue.

Economic calculations

Data for the economic calculations are based on the investment and maintenance costs of pilot farm 1 in GWB. Since pilot farm 1 was a scientific mussel farm and therefore without annual running cost (that would otherwise be faced by a commercial business), supplementary data were derived from a commercial mussel farm in Kiel Fjord (Krost et al., 2011).

Krost et al. (2011) predicted annual yields of 25 t and 100 t of mussels for human consumption after 18 months. Annual running costs include anchoring and foundation, longlines, buoys, floaters, socks, collectors, and staff. The economic lifetime varied between 1 and 5 years. Investment costs covering a boat and machinery (both with an assumed lifetime of 5 years), as well as a land station, were summarized under annual investment costs. Since staff is the dominating cost factor, the salaries from the year 2010 (Krost et al., 2011) were recalculated for the year 2020 assuming an increase of 30% (the statistical average salary increase in Germany). With increasing farm size, we assumed that staff and investment costs decrease steadily per produced ton of mussels; this decrease is relatively high in smaller farms and negligible in very large units.

The salinity in GWB only allows for the production of mussels for mussel meal or feed, harvested after about 12 months of cultivation time. As a consequence, we assumed lower production costs with a reduced staff effort of 50% and 2% lower investment costs. These numbers are based on our own experiences with our two small pilot farms and verified by discussions with experts from the commercial mussel farm sector and literature.

The annual production of feed mussels in GWB is assumed to be 0.278 kg m⁻³ cultivation volume. This data is based on a model simulation study in Buer et al. (2020) and verified by our experimental farms. Assuming a cultivation volume from the surface to a depth of 3 m, and taking into account the relatively low productivity, a farm producing 100 t mussels per year would cover a surface area of about 120 ha. The nitrogen (phosphorus) content in mussels is assumed to be 0.008 (0.0006) kg kg⁻¹ fresh mussels, based on the cultivated mussels in GWB.

In addition to the production of feed mussels, we assumed a compensation for nutrient extraction based on the removal costs of a wastewater treatment plant (WWTP). The revenue for nitrogen and phosphorus removal is set at 30,000 € t⁻¹ and 80,000 € t⁻¹ (COWI, 2007; Gren, Jonzon & Lindqvist, 2008; Hautakangas et al., 2014).

Bio-chemical status of coastal waters

Although all nine study sites were similar, their ecological status and its temporal development differed strongly (Fig. 3). The majority had average annual TN concentrations between 20–50 µmol l⁻¹, TP concentrations between 1–2 µmol l⁻¹, and Chl. a concentrations between 5–20 mg m⁻³. Consequently, all coastal waters were regarded as eutrophic, their ecological status was classified as unsatisfactory (LUNG 2013), and a need for measures to improve water quality was apparent. During the 1990s, the technical improvement of WWTPs caused a strong reduction of nutrient loads to coastal waters in the Federal State of Mecklenburg-Vorpommern, Germany. The largest five WWTPs reduced TP loads by more than 95% and TN loads by over 80% (LUNG 2013). As a result, the riverine loads declined by about 70% (TP). A significant decline in TN loads did not take place during the last 30 years. The riverine loads closely correlate with the river discharge. This is true for the TP loads after 1996, as well (LUNG 2013). In seven of the coastal waters, the load reductions during the 1990s caused a decline in TN and TP annual concentrations (Fig. 3), but only two showed reductions in Chl. a concentrations and only three increased water transparency. After 2000, the nutrient concentrations in the coastal waters did not indicate significant changes. Since the riverine loads were largely stable during the past decades, it can’t be expected that a reduction in nutrients in coastal waters will take place in the future without new, additional measures. Further, it seems unrealistic that additional external load reductions will be implemented

After 2000, the Chl. a concentrations did not show a significant decline. In most coastal waters, positive effects on water transparency were not visible either. Exceptions were the Barther Bodden, the Jasmunder Bodden, and the Warnow Estuary. It is very likely that the status of the two Bodden waters improved as a result of reduced diffuse agricultural nutrient loads. The Warnow Estuary, as a shipping channel, was subject to several dredging activities. This increased the water exchange with the Baltic Sea and reduced the nutrient and Chl. a levels. In general, the nutrient and Chl. a levels seem directly related to the water exchange time and the shallowness of systems. A low water exchange time and a large euphotic zone (low average water depth) are likely reasons for the very high nutrient and Chl. a concentrations in the Kleiner Jasmunder and the Barther Bodden, as well. On the other hand, the relatively strong reductions in nutrients and Chl. a concentrations in both water bodies over the last decades indicate a distinct reaction to changes in loads. The water exchange time and the average depths are parameters that determine the effectiveness of internal measures in coastal waters.

The sensitivity of aquatic systems is one factor that determines how promising a potential internal measure will be. Another factor is the present state of pollution and its deviation from the good ecological status. Figure 3 indicates the desired threshold values, according to the WFD for each coastal water. Wismar Bay and Salzhaff are already close to a good status and efforts to reduce diffuse loads might already be enough to meet the threshold. While for the Warnow Estuary, the West/Nord Rügener Bodden, and Strelasund and Greifswalder Bodden it seems possible to meet the good status, it would require additional internal measures. Thanks to its size and importance for fishing and recreating, the Greifswalder Bodden is the best case study for assessing the suitability of mussel farming to improve ecological status.

Seasonal nutrient and chlorophyll relationships

During the winter, primary production in Baltic coastal waters is limited by temperature and light. The increase of Chl. a concentrations and decrease of dissolved inorganic nutrient concentrations that takes place during the spring and summer indicates that nutrients become a potentially limiting resource for phytoplankton biomass in most water bodies (Table 2). In all coastal waters, DIN concentrations strongly decline between late winter and summer. For DIP, the decline takes place earlier and by March concentrations are low. The molar N/P ratio of 16 (according to Redfield) provides a rough estimate for which nutrient is limiting primary production.

During March and April, high nitrogen discharges initiate blooms in coastal waters; the average DIN:DIP ratio ranged from 26 to 720, indicating a P limitation (Table 2). In May, most water bodies show a shortage of DIP. In June, phytoplankton growth reliance begins to change towards a shortage of N. During July, the majority of the waterbodies show an average DIN:DIP ratio between 2–10, indicating an N shortage. In the Wismar Bay, Nord/West Rügener Bodden, and Strelasund and Greifswalder Bodden, this situation remained the same through August and September (Table 2), whereas the Salzhaff and Warnow Estuary returned to an N/P ratio of close to 16:1 during this time. Only the shallow Kleiner Jasmunder Bodden and the Barther Bodden were exceptions. Here, the Chl. a concentrations decreased from May until July and absolute dissolved inorganic nutrient concentrations fluctuated but were relatively high (Table 2). Results indicate that phytoplankton growth is not controlled by the availability of nutrients but rather by other parameters, such as turbidity and light.

The GWB is representative of coastal waters due to its short availability of P in the spring and a shortage of N between July and September.

This is shown for GWB in Fig. 4. Between March and September, the Chl. a concentration shows a close positive correlation to TN and TP concentrations.

This has several implications: (1) nutrients have a controlling function for phytoplankton biomass and as a consequence, measures that reduce nutrient concentrations in the water (such as mussel farming) will cause a reduction in phytoplankton concentrations and have a positive effect on water quality; (2) especially between July and September, the availability of N seems to control the productivity; summer is exactly the time when mussels show the fastest growth and are most efficient at removing nutrients from the water column via phytoplankton filtration and uptake.

Improvement of water quality during summer

Chl. a concentration and Secchi depth are related during the summer (the main grow out season for mussels) and therefore directly connected to the mitigation process of mussel farming. The linear regression shows a strong negative relationship between total nitrogen and Chl. a concentrations during July up until September (Fig. 5A). Secchi depth can be better explained by Chl. a than total suspended solid concentration (TSS) (Figs. 5B, 5D). Autocorrelation between TSS concentration and phytoplankton biomass results in a close regression coefficient because biomass is a natural part of TSS. The stronger coefficient of determination, however, affirms that Secchi depth can be better described by Chl. a concentration. Based on the prior linear regression model between TN and Chl. a concentration, a regression model describing the relationship between TN and Secchi depth was established to describe water quality improvements when nitrogen is mitigated (Fig. 5C).

According to linear regression model A (Fig. 5), Chl. a concentration can be reduced to approx. 1.4 mg m⁻³ if total nitrogen concentration is reduced to the threshold value of 16.9 µmol l⁻¹. Based on the relationship between Secchi depth and TN concentration (C), Secchi depth would increase by approx. 70 cm. Given that GWB has a monthly water exchange rate, the reduction effort has to be accomplished on a monthly basis.

Monthly nitrogen reductions would result in annual values of 41.6 µmol l⁻¹ TN and 10.6 mg m⁻³ Chl. a concentration, accounting for a reduction of 15.5% TN and 29.8% Chl. a of the mean annual concentration.

Water quality improvement by mussel farming

In situ investigations of clearance rates (CR) of blue mussels from the two pilot farms showed overall low clearance rates compared to laboratory CR investigations. Mytilus spp. from the pilot farm 2 showed slightly higher CRs at a lower ambient Chl. a concentration (15 mg m⁻³) than Mytilus spp. from pilot farm 1 with a higher ambient Chl. a concentration (22 mg m⁻³). Laboratory tests revealed a significant decrease in CR with increasing Chl. a concentration exceeding 20 mg m⁻³ (Fig. 6A). Based on these results, Chl. a is an important driver effecting blue mussel CRs.

Nutrient contents of the mussels (wet weight total) did not differ significantly between both pilot farms, indicating that neither salinity nor Chl. a concentration influence the nutrient content (Fig. 6B).

Rapid growth rates in the first few months lead to high nutrient extraction capacities per month. The first settling of mussel larvae at pilot farm 1 was recorded in July. During August, juvenile mussels had an average total wet weight of 17.78 ± 5.44 mg per mussel, while in September the average wet weight already reached 147.01 ± 28.40 mg per mussel. During August and September, TN concentrations in GWB ranged between 41.5 to 40.0 µmol l⁻¹ (equaling approx. 1,700 t N within GWB).

Subsequently, if 50% of the GWB was covered with mussel farms, it would take up 257 t N and reduce TN concentration to 34.6 µmol l⁻¹ by September (Table 3). According to the linear regression model (Table 3C), reduced nitrogen would increase the Secchi depth by 7.83 cm. Our results also show that if mussel farming is used locally in areas with a low water exchange rate, the effect of mussel farming can be extended. Based on the other water bodies that have no direct water exchange with the Baltic Sea (Table 1), we assumed that the Hagnesche Wiek (location of pilot farm 1 (Fig. 1)) has a lower water exchange rate of approx. 6–7 a⁻¹. Here, the results show that the TN concentration could be reduced to 32.1 µmol l⁻¹ and Secchi depth would increase by 10.6 cm (Table 3).

In addition to water transparency improvements seen by reducing nitrogen concentration, the mussels improve water transparency by removing phytoplankton. Taylor et al. (2020, in submission) calculated an average depletion of 5% from autumn 2017 to summer 2018 for pilot farm 1. According to the linear regression model (Fig. 5B), the reduction of Chl. a concentration from a mussel farm occupying 50% would increase Secchi depth by an additional 13.3 cm, resulting in a total improvement of ∼20 cm.

Our results clearly show that the cultivation of small sized mussels in low salinity environments must cover a substantial amount of surface area to have a severe impact on water quality. This, however, can create a tradeoff between potential improvements in water quality and negative effects emerging from the mussel farm.

Potential negative ecological effects of mussel cultivation in GWB

The primary negative effects of suspended mussel cultivation are nutrient enrichment of benthic habitats and the spread of pathogens.

While sediment TOC was not significantly influenced by the mussel farm in GWB (Fig. 7), during 2018 an increasing trend of TOC was indicated beneath the pilot farm. This might be explained by the fact that during 2018, the mussel farm was fully stocked (resulting in a higher bio deposition rate). Additionally, by the end of the summer, 80% of the mussel stock was lost after mussels detached and sunk, inadvertently increasing overall organic content at the seafloor.

Bio deposition was higher over the summer at pilot farm 1 than at the reference site. This was also confirmed by results from the Kiel Farm (Fig. 7). Results obtained from the commercial farm, however, showed lower bio deposition compared to GWB, even though the commercial farm was bigger in size and stock density. It has to be mentioned that measurements were not obtained at the same time. While GWB measurements were taken in June, measurements at the commercial farm were taken in October. Therefore, it can be assumed that in GWB the sedimentation of phytoplankton adds to the content of bio deposition produced by mussels, leading to significant increased values.

The Vibrio spp. concentration in cultivated blue mussels was 1.07 10⁴ ±1.75 10³ CFU g⁻¹ (Fig. 8). Higher concentrations of Vibrio spp. were found in the surface water and sediment at the reference points. However, sediment trap samples showed increased Vibrio spp. concentrations in the pilot farm 1 compared (Fig. 8).

The results show that Vibrio bacteria are concentrated in feces and pseudo feces in the water column within the mussel farm, and concentrations in sediments are lower. This may be an indication that bio deposits are further distributed and not concentrated directly beneath the mussel farm.

Economic assessment of mussel cultivation in GWB

Based on the expected mussel yields in GWB, our results show that mussel mitigation with the revenues from feed mussel sales and nutrient removal will not be profitable in GWB (Fig. 9). Even though annual costs decreased with increasing production volume, the net balance remained negative. Revenues from nutrient reduction can only narrow the gap towards cost neutrality. In GWB, cost neutrality is not reached because the small sized mussels can only be sold as feed mussels for a minor sales price of 0.06 € kg⁻¹. In comparison, fresh blue mussels for human consumption could be sold for 11.0 € kg⁻¹. According to Buer et al. (2020a), mussel cultivation for human consumption is only possible at a salinity threshold of 12 PSU, indicating that mussel mitigation in Wismar Bay and Salzhaff and Warnow Estuary could be profitable if mussels can be sold for human consumption instead of animal feed.

In GWB, a farm size of approx. 200 ha would reduce the cost gap to under 1,000 €. This gap could be closed if water transparency improvements were compensated, as well.

Depending on the production volume, nutrient removal costs would range between 40 to 814 € kg N⁻¹ and 899 to 18,000 € kg P⁻¹. Even if mussel production volume increases, nitrogen extraction by mussels is more expensive than other land-based measures (Fig. 9B). Mussel mitigation becomes logical when nutrient pollution is caused by internal processes or when land-based measures have reached their feasibility limit.