Blue mussel beds as biodiversity hotspots on the rocky shores of the northern Baltic Sea

ABSTRACT The Baltic Sea is a vulnerable ecosystem currently undergoing a number of changes, both natural and human induced. The changes are likely to affect the species found on these shores, e.g. their distribution and interactions with other species. Blue mussels (Mytilus trossulus x Mytilus edulis) provide one of the main biogenic hard structures on the shallow shores of the Baltic Sea where they aggregate into dense beds and provide a number of resources for over 40 associated macrofaunal species, thus functioning as ecosystem engineers. The blue mussel, being a marine species, is highly likely to be affected by any changes in sea water salinity, circulation and/or water balance. These changes could trickle down also to affect the associated macrofaunal communities. The aims of this thesis were three-fold: first, I examined and described the macrofaunal communities found within blue mussel patches since the fauna associated with mussel patches had never been described in the study area prior to this thesis. Second, I explored how changes in mussel density, size as well as patch size and shape would affect the mussel communities. Finally, I tested how general landscape theories derived from terrestrial studies function in blue mussel systems. Theories included the structural heterogeneity hypothesis, species-area relationships, edge effects and patch isolation effects. The work shows that blue mussels in the northern Baltic Sea have an indisputable function as diversity hotspots and that the faunal assemblages found in mussel patches are extremely rich and unique. Further on, it shows that changes in mussel biomass, size, patch size and amount of edge have the potential to alter the faunal assemblages and diversity within patches. Finally, it shows that although some landscape theories, such as the structural heterogeneity hypothesis, seem to apply also in blue mussel communities, others cannot be directly applied due to the different prevailing conditions in the study system. This is a pioneering work looking at diversity shaping processes on the rocky shores of the Gulf of Finland, making up over 40% of the total water basin. A focus on niche construction, positive facilitation effects and ecosystem engineering could provide new insights and methods for conservation biology, but before this can be done, we need to fully understand the circumstances under which a species becomes an ecosystem engineer and recognize the systems in which it functions.

Assessing the sensitivity of blue mussel beds to pressures associated with human activities.

The Joint Nature Conservation Committee (JNCC) commissioned this project to generate an improved understanding of the sensitivities of blue mussel (Mytilus edulis) beds, found in UK waters, to pressures associated with human activities in the marine environment. The work will provide an evidence base that will facilitate and support management advice for Marine Protected Areas, development of UK marine monitoring and assessment, and conservation advice to offshore marine industries. Blue mussel beds are identified as a Habitat of Principle Importance (HPI) under the Natural Environment and Rural Communities (NERC) Act 2006, as a Priority Marine Feature (PMF) under the Marine (Scotland) Act 2010, and included on the OSPAR (Annex V) list of threatened and declining species and habitats. The purpose of this project was to produce sensitivity assessments for the blue mussel biotopes included within the HPI, PMF and OSPAR habitat definitions, and clearly document the supporting evidence behind the assessments and any differences between them. A total of 20 pressures falling in five categories - biological, hydrological, physical damage, physical loss, and pollution and other chemical changes - were assessed in this report. The review examined seven blue mussel bed biotopes found on littoral sediment and sublittoral rock and sediment. The assessments were based on the sensitivity of M. edulis rather than associated species, as M. edulis was considered the most important characteristic species in blue mussel beds. To develop each sensitivity assessment, the resistance and resilience of the key elements are assessed against the pressure benchmark using the available evidence gathered in this review. The benchmarks were designed to provide a ‘standard’ level of pressure against which to assess sensitivity. Blue mussel beds were highly sensitive to a few human activities: • introduction or spread of non-indigenous species (NIS); • habitat structure changes - removal of substratum (extraction); and • physical loss (to land or freshwater habitat). Physical loss of habitat and removal of substratum are particularly damaging pressures, while the sensitivity of blue mussel beds to non-indigenous species depended on the species assessed. Crepidula fornicata and Crassostrea gigas both had the potential to outcompete and replace mussel beds, so resulted in a high sensitivity assessment. Mytilus spp. populations are considered to have a strong ability to recover from environmental disturbance. A good annual recruitment may allow a bed to recovery rapidly, though this cannot always be expected due to the sporadic nature of M. edulis recruitment. Therefore, blue mussel beds were considered to have a 'Medium' resilience (recovery within 2-10 years). As a result, even where the removal or loss of proportion of a mussel bed was expected due to a pressure, a sensitivity of 'Medium' was reported. Hence, most of the sensitivities reported were 'Medium'. It was noted, however, that the recovery rates of blue mussel beds were reported to be anywhere between two years to several decades. In addition, M. edulis is considered very tolerant of a range of physical and chemical conditions. As a result, blue mussel beds were considered to be 'Not sensitive' to changes in temperature, salinity, de-oxygenation, nutrient and organic enrichment, and substratum type, at the benchmark level of pressure. The report found that no distinct differences in overall sensitivity exist between the HPI, PMF and OSPAR definitions. Individual biotopes do however have different sensitivities to pressures, and the OSPAR definition only includes blue mussel beds on sediment. These differences were determined by the position of the habitat on the shore and the sediment type. For example, the infralittoral rock biotope (A3.361) was unlikely to be exposed to pressures that affect sediments. However in the case of increased water flow, mixed sediment biotopes were considered more stable and ‘Not sensitive’ (at the benchmark level) while the remaining biotopes were likely to be affected.

Using a clearly documented, evidence-based approach to create sensitivity assessments allows the assessment basis and any subsequent decision making or management plans to be readily communicated, transparent and justifiable. The assessments can be replicated and updated where new evidence becomes available ensuring the longevity of the sensitivity assessment tool. For every pressure where sensitivity was previously assessed as a range of scores in MB0102, the assessments made by the evidence review have supported one of the MB0102 assessments. The evidence review has reduced the uncertainty around assessments previously undertaken in the MB0102 project (Tillin et al., 2010) by assigning a single sensitivity score to the pressures as opposed to a range. Finally, as blue mussel bed habitats also contribute to ecosystem function and the delivery of ecosystem services, understanding the sensitivity of these biotopes may also support assessment and management in regard to these. Whatever objective measures are applied to data to assess sensitivity, the final sensitivity assessment is indicative. The evidence, the benchmarks, the confidence in the assessments and the limitations of the process, require a sense-check by experienced marine ecologists before the outcome is used in management decisions.

Fauna associated with Bathymodiolus azoricus mussel beds within hydrothermal fields of the Mid-Atlantic Ridge

Structure of assemblages associated with mussel aggregations of Bathymodiolus azoricus was investigated. Mussel beds were found on hydrothermal vent fields on the Mid-Atlantic Ridge (Menez Gwen, Lucky Strike, and Rainbow) at depths 850-2400 m. The community structure of the mussel bed assemblages varied between studied areas. Large number of species was unique to mussel beds of the Menez Gwen field; the most observed taxa were not specialized hydrothermal species. All other nonunique species were found within the Lucky Strike region. The lowest mussel assemblage structure evenness was observed in the shallowest Menez Gwen area (850 m depth). We assume that two types of mussel assemblages (nematode-dominated and copepod-dominated) exist within the Lucky Strike field. The assemblages of B. azoricus differ significantly from assemblages of B. thermophilus inhabiting Pacific hydrothermal vents.

Benthic fauna associated with mussel beds and shrimp swarms within hydrothermal fields on the Mid-Atlantic Ridge

Macrofaunal assemblages with prevalence of Bresiliidae shrimps and Mytilidae mussels are abundant in at hydrothermal vents along the Mid-Atlantic Ridge. Mussels inhabit zones of diffuse seeps of hydrothermal fluids with temperature abnormalities up to several degrees. Shrimps inhabit an extreme biotope in a mixed interface between seawater and hydrothermal fluids at temperature up to 20-30°C. We studied the mussel and shrimp assemblages in three hydrothermal vent fields: Rainbow, Broken Spur, and Snake Pit. Species richness of the mussel assemblages within at least two fields (Broken Spur and Snake Pit) is higher as compared with shrimps from the same hydrothermal vent fields. Fauna inhibiting shrimp swarms lack almost any taxa specific for particular assemblages: almost all the taxa are also present in the mussel beds. Structure of the shrimp assemblage is less homogeneous as compared with that of the mussel assemblage. Population prevalence of one taxon (Copepoda) in the shrimp assemblage is most likely connected with extreme and unstable conditions of the biotope occupied by the shrimps in a hydrothermal field. Taxonomic similarity between the mussel and shrimp assemblages within one hydrothermal vent field is higher as compared with similarity between the mussel (or shrimp) assemblages from different fields.

Mussel Community Studies [Year One].

Mytilus californianus communities (mussel beds) were examined from six geographic localities in Southern California. These included two mainland sites, Coal Oil Point and San Diego; and four island sites, San Miguel, Santa Cruz, San Nicholas, and Santa Barbara Islands. Optimal sample sizes were determined for each locality. In general, a sample, size of 1500 cm2 (five cores) was optimal for the "typical" mussel bed. However, structurally unique mussel beds required individual consideration. Community biomass, diversity, species richness, and species evenness were calculated quarterly for the island localities and biannually for mainland locations. The molluscs, primarily the mussels, accounted for 90% of the total biomass while all other groups combined accounted for 10% or less of the total biomass. The mussel communities from all localities contributed to the master species list which conservatively contained 346 species. The most diverse localities were Coal Oil Point and Santa Cruz Island with an average number of 73 and 74 species/O.lS m respectively. No overall seasonal patterns existed in community composition. The community similarity analyses showed the mainland localities biotically dissimilar from the islands and both groups were characterized by distinct faunal assemblages. In addition, San Miguel Island biota were unique among the island sites. The most important mussel bed structural attributes provided habitats for the associated community and included sediment and coarse fraction features. Food-related resources provided by the mussel bed were secondarily important. Community diversity generally increased with the quantity of habitat and food resources. (PDF contains 138 pages)

Mussel Community Studies [Year Two].

The communities associated with Mytilus californianus (mussel) beds from eleven geographic localities in Southern California were examined. The localities included four mainland sites - Government Point, Goleta Point, Corona del Mar and San Diego; and seven offshore islands including - San Miguel Island, Santa Rosa Island, Santa Cruz Island, Santa Barbara Island, Santa Catalina Island, San Nicholas Island and San Clemente Island. This geographic coverage. was much more complete than the previous year (1975-1976 program). However, it is still less than ideal. In particular a single island collection locality may not be representative of an entire island. Therefore greater geographic coverage of the islands is recommended for the future. In general, the 1500 cm2 sample size adopted during the 1975-1976 program proved adequate for sampling most of the structurally diverse mussel beds this year. This sample size supplied information on the characteristic and abundant species inhabiting a particular mussel bed, and provided data which was well suited to intersite community comparisons. This sample size was too small in several instances to include the rarer, less abundant species. The mussel communities from all localities contributed to the master species list which contained conservatively 481 species of animals and 63 specie s of algae. The most diverse collections came from Santa Cruz Island and Corona del Mar, and these areas contained 120 and 119 species respectively. The lowest diversity was recorded for the mussel beds from Goleta Point: which contained 57 species. Mussel community samples were collected from upper and lower intertidal areas occupied by the mussel beds within a locality. In general, community differences both in composition and abundance were associated with these collections. (PDF contains 158 pages)

Mussel Community Studies [Year Three].

The communities associated with Mytilus californianus (mussel) beds from 20 geographic sites in southern California were examined. The study areas included six mainland sites - Government Point, Goleta Point, Ventura, Corona del Mar, Carlsbad, and San Diego,and two sites on opposite sides of seven offshore islands - San Miguel Island, Santa Rosa Island, Santa Cruz Island, Anacapa Island, San Nicholas Island, Santa Cruz Island and San Clemente Island. : The mussel communities from all areas contributed to the master species list which now encompasses conservatively, 610 species of animals and 141 species of algae. The most diverse collection came from Cat Rock, Anacapa Island where the mussel beds supported 174 species of invertebrates. The lowest diversity was recorded for mussel beds from Ben Weston, Santa Catalina Island which contained 46 species. In general, the island mussel beds supported a greater diversity of both animals and plants. Mussel community samples were collected from upper and lower intertidal areas occupied by the mussel beds within a locality. Community differences in both composition and abundance were associated with these collections. Overall. community similarity analysis revealed five major patterns which corresponded to characteristic species assemblages occupying the mussel beds from the various geographic areas. The patterns included: (1) clusters of localities which display a north-south geographic pattern with respect to the similarity of their respective mussel communities, (2) a separation of selected island and mainland communities because of dissimilarities in their species composition, (3) differences between mussel communities. on opposite sides of the offshore islands, (4) clusters of species whose highest abundances characterize selected localities, (5) species groups ubiquitous to all mussel beds examined. The results of the community analysis further suggest that predictions can be made delineating the probable mussel community inhabitants of areas not sampled. The species distribution patterns observed appear to correspond in part to the influence of currents and water masses which bear planktonic larvae and impinge on selected localities. The most important mussel bed features associated with community differences were quantitative and qualitative differences in the potential microhabitats. Those features associate~ with greater species diversity include the pore base of coarse fraction shell and rock debris, skewness and kurtosis of the sediment grain-size distributions and mussel bed thickness. Those features associated with lower species diversity included the quantity of tar. and rock and shell debris trapped within the mussel bed. (PDF contains 51 pages)

Shore exposure affects mussel population structure and mediates the effect of epibiotic algae on mussel survival in SW Ireland

On rocky shores, the relative importance of abiotic and biotic processes that regulate community structure are thought to vary with levels of shore exposure. This can lead to characteristic features found on sheltered and exposed shores. This study identified differences in the population structure of mussels on exposed and sheltered rocky shores on Atlantic coasts of south-west Ireland. Direct interactions between epibiotic algae and their host mussels were also examined to test if potential effects varied with shore exposure. Mussel beds on sheltered shores were less dense and comprised larger mussels with greater rates of individual survival and growth than those on exposed shores. The results of a field experiment showed that algal epibionts had a negative effect on mussel survival on sheltered shores but not on exposed shores. Surprisingly, the presence of algal epibionts had no effect on mussel growth on either shore type. These findings contrast with those of previous studies. The effects of shore exposure and algal epibionts on Mussels may be species-specific and may interact with other factors across different regions. This study shows that predictions of effects of exposure on mussel populations and their epibionts should only be based on specific experimental evidence and cannot be generalised across regions. (C) 2009 Elsevier Ltd. All rights reserved.

Do mussel patches provide a refuge for algae from grazing gastropods?

On rocky shores, cover of macroalgae is often greater growing epibiotically on mussels compared to algae growing directly attached to rock. A survey of two shores on the east coast of Ireland confirmed that mussel beds contained greater percentage algal cover and more diverse algal assemblages compared to those on rock. The reasons for this difference are not clear. It has been suggested that mussel beds provide a refuge for algae from grazing gastropods. Surprisingly, we found no evidence to support this. Using wax discs, gastropod grazing patterns were found to be similar within the mussel beds as on rock. The mussel beds do not appear to provide a refuge for algae from grazing activity at this scale and we suggest other possible mechanisms for the prevalence of epibiotic algal cover on mussels. Intertidal grazers may in fact affect the epibiotic algae on mussels and thereby affect indirectly the persistence of mussel beds.

Effects of baited crab pots on cultivated mussel (Mytilus edulis) survival rates

The shore crab, Carcinus maenas, is recognized as a voracious predator of blue mussels, Mytilus edulis, having the potential to greatly reduce stocks in the benthic cultivation industry. As a consequence, baited crab pots are often deployed on and around cultivated benthic mussel beds to trap and remove crabs, in an attempt to reduce predatory pressure. Little is known about how C. maenas behaves around crab pots, but for many other crustacean fisheries, the trapping efficiency of pots is often low. Crabs may be attracted towards but not enter pots, instead feeding on cultivated mussels outside pots on the surrounding substratum. We tested whether the rate of loss of mussels attached to plates differed in areas next to baited pots compared with unbaited pots and to areas without any pots, at two sea loughs (60 km apart) in Northern Ireland. In Strangford Lough, more mussels were lost from plates next to baited pots than the other treatments. In Carlingford Lough, however, we found no difference in the number of mussels lost from plates in any treatment. This difference could be attributed to the different assemblages of mobile benthic predators at the two loughs. The presence of the starfish Asterias rubens, which was absent from experimental sites in Carlingford Lough, was thought to be responsible for increased predation rates near baited pots in Strangford. It is, therefore, important to consider local predator communities when deploying crab pots as a predator mitigation technique to ensure predation rates are in fact reduced and not enhanced. This study is of relevance not only to attempts to limit predation on commercial stocks of benthic cultivated mussels but also in situations where baited traps are deployed close to species vulnerable to mobile benthic predators.

Population dynamics of blue mussels in a variable environment at the edge of their range

Spatial and temporal variation in the abundance of species can often be ascribed to spatial and temporal variation in the surrounding environment. Knowledge of how biotic and abiotic factors operate over different spatial and temporal scales in determining distribution, abundance, and structure of populations lies at the heart of ecology. The major part of the current ecological theory stems from studies carried out in central parts of the distributional range of species, whereas knowledge of how marginal populations function is inadequate. Understanding how marginal populations, living at the edge of their range, function is however in a key position to advance ecology and evolutionary biology as scientific disciplines. My thesis focuses on the factors affecting dynamics of marginal populations of blue mussels (Mytilus edulis) living close to their tolerance limits with regard to salinity. The thesis aims to highlight the dynamics at the edge of the range and contrast these with dynamics in more central parts of the range in order to understand the potential interplay between the central and the marginal part in the focal system. The objectives of the thesis are approached by studies on: (1) factors affecting regional patterns of the species, (2) long-term temporal dynamics of the focal species spaced along a regional salinity gradient, (3) selective predation by increasing populations of roach (Rutilus rutilus) when feeding on their main food item, the blue mussel, (4) the primary and secondary effects of local wave exposure gradients and (5) the role of small-scale habitat heterogeneity as determinants of large-scale pattern. The thesis shows that populations of blue mussels are largely determined by large scale changes in sea water salinity, affecting mainly recruitment success and longevity of local populations. In opposite to the traditional view, the thesis strongly indicate that vertebrate predators strongly affect abundance and size structure of blue mussel populations, and that the role of these predators increases towards the margin where populations are increasingly top-down controlled. The thesis also indicates that the positive role of biogenic habitat modifiers increases towards the marginal areas, where populations of blue mussels are largely recruitment limited. Finally, the thesis shows that local blue mussel populations are strongly dependent on high water turbulence, and therefore, dense populations are constrained to offshore habitats. Finally, the thesis suggests that ongoing sedimentation of rocky shores is detrimental for the species, affecting recruitment success and post-recruit survival, pushing stable mussel beds towards offshore areas. Ongoing large scale changes in the Baltic Sea, especially dilution processes with attendant effects, are predicted to substantially contract the distributional range of the mussel, but also affect more central populations. The thesis shows that in order to understand the functioning of marginal populations, research should (1) strive for multi-scale approaches in order to link ecosystem patterns with ecosystem processes, and (2) challenge the prevailing tenets that origin from research carried out in central areas that may not be valid at the edge.