Bioinvasion threatens the genetic integrity of native diversity and a natural hybrid zone: smooth‐shelled blue mussels (Mytilus spp.) in the Strait of Magellan

Smooth‐shelled blue mussels of the Mytilus edulis species complex are widely distributed bivalve molluscs whose introductions threaten native marine biodiversity (non‐indigenous species – NIS). The aim of the present study was to identify the species and hybrids of Mytilus present in the Magellan Region (southern Chile). Results indicate that three mussel species of the Mytilus edulis complex are found in the region – M. edulis, M. chilensis (or the Southern Hemisphere lineage of Mytilus galloprovincialis), and M. galloprovincialis of Northern Hemisphere origin. For the first time, alleles of the introduced M. trossulus are reported from the Southern Hemisphere. In the Strait of Magellan the native Pacific blue mussel, Mytilus chilensis and the native Atlantic blue mussel, Mytilus edulis, meet and mix at a natural hybrid zone (about 125 km in length). This is the first record of a natural Mytilus hybrid zone in the Southern Hemisphere and is also the first record of the co‐occurrence of genes from all four Mytilus species in any one region. These results contribute to the knowledge of the biodiversity and delimitation of mussel species in southern South America, and highlight how introduced species may threaten the genetic integrity of native species through hybridization and introgression.     

Mussel beds — amensalism or amelioration for intertidal fauna?

The faunal assemblages of a mussel bed (Mytilus edulis L.) and ambient sandflat were compared to study how a bioherm of suspension feeding organisms affects benthic communities in a tidal flat. During a survey of mussel beds in the Wadden Sea at the island of Sylt (North Sea), a total of 52 macrofaunal species and 44 meiobenthic plathelminth species were detected. They occupied different microhabitats in the mussel bed. 56% of the macrofauna species were dwelling in the sediment beneath the mussels and 42% were epibenthic or epiphytic. The latter were restricted in their occurrence to the mussel bed. Along a transect from the sandflat to the mussel bed the mean species densities of macrofauna did not differ significantly, while abundances were significantly lower in the mussel bed than in the sandflat. The composition of the assemblages shifted from a dominance of Polychaeta in the sandflat to Oligochaeta in the mussel bed. Surface filter-feeding polychaetes of the sandflat (Tharyx marioni) were displaced by deposit feeding polychaetes under the mussel cover (Capitella capitata, Heteromastus filiformis). The total meiobenthic density was lower and single taxa (Ostracoda, Plathelminthes, Nematoda) were significantly less abundant in the mud of the mussel bed. The plathelminth assemblage was dominated by grazing species (Archaphanostoma agile), and differed in community structure from a sandflat aseemblage. An amensalistic relationship was found between the suspension-feeding mussels and suspension-feeding infauna, while deposit-feeders were enhanced. The presence of epibenthic microhabitats results in a variety of trophic groups co-occurring in a mussel bed. This is hypothesized as trophic group amelioration and described as an attribute of heterotrophic reefs.     

Documentation of sites of intertidal blue mussel (Mytilus edulis L.) beds of the Lower Saxonian Wadden Sea, southern North Sea (as of 2003) and the role of their structure for spatfall settlement

Field surveys (dating back to 1950) and aerial photograph series (dating back to 1966) were evaluated to determine sites of intertidal blue mussel (Mytilus edulis) beds at the Wadden Sea coast of Lower Saxony. Maps were prepared indicating sites of blue mussel beds during the last decades. A table gives additional information on the presence (or absence) of blue mussel beds at each site at the time of large-scale surveys. Altogether 187 sites of M. edulis beds were recorded in the investigation area. In spring 1996, there were still only 19 sites where mussel beds still occurred, although at 51 sites residual mussel-bed structures were present, e.g. shell bases of former beds or protruding patches (which had been occupied by M. edulis before the beds vanished) and open spaces. At that time, the majority of the sites contained neither mussel beds nor mussel-bed structures. The analysis of recent data confirmed that mussel larvae have preferred to settle in sites of present mussel beds and sites with bases of former mussel beds. There was no preferential selection of one of these categories (settled beds vs. shell bases). On the other hand, the presence of mussel beds or mussel bed structures is not obligatory for settlement, because sites without those structures were also re-settled by the spatfall in 1996, even though on a smaller scale.     

Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia

The transport and establishment of non-indigenous species in coastal marine environments are increasing worldwide, yet few studies have experimentally addressed the interactions between potentially dominant non-native species and native organisms. We studied the effects of the introduced mussel Musculista senhousia on leaf and rhizome growth and shoot density of eelgrass Zostera marina in San Diego Bay, California. We added M. senhousia over a natural range in biomass (0–1200 g dry mass/m²) to eelgrass in transplanted and established beds. The effects of the non-indigenous mussel varied from facilitation to interference depending on time, the abundance of M. senhousia, and the response variable considered. Consistent results were that mussel additions linearly inhibited eelgrass rhizome elongation rates. With 800 g dry mass/m² of M. senhousia, eelgrass rhizomes grew 40% less than controls in two eelgrass transplantations and in one established eelgrass bed. These results indicate that M. senhousia, could both impair the success of transplantations of eelgrass, which spread vegetatively by rhizomes, and the spread of established Z. marina beds to areas inhabited by M. senhousia. Although effects on leaf growth were not always significant, in August in both eelgrass transplantations and established meadows leaf growth was fertilized by mussels, and showed a saturation-type relationship to sediment ammonium concentrations. Ammonium concentrations and sediment organic content were linear functions of mussel biomass. We found only small, non-consistent effects of M. senhousia on shoot density of eelgrass over 6-month periods. In established eelgrass beds, but not in transplanted eelgrass patches (≈0.8 m in diameter), added mussels suffered large declines. Hence, eelgrass is likely to be affected by M. senhousia primarily where Z. marina beds are patchy and sparse. Our study has management and conservation implications for eelgrass because many beds are already seriously degraded and limited in southern California where the mussel is very abundant. Received: 31 May 1997 / Accepted: 4 September 1997     

Wadden Sea mussel beds invaded by oysters and slipper limpets: competition or climate control?

Introduced species are often considered to be a threat to residents, but not all reciprocal trends may reflect species interaction. In the northern German Wadden Sea, native mussel Mytilus edulis beds are declining and overgrown by introduced Pacific oysters Crassostrea gigas and slipper limpets Crepidula fornicata. We review the population development of the three species and analyse whether the invading species may be responsible for the decline of native mussels. The Pacific oyster predominately settles on mussel beds in the intertidal and the slipper limpet dominates around low water line. We compare the development of mussels and invaders in two subregions: mussel beds near the islands of Sylt and Amrum decreased both in the presence (Sylt) and absence (Amrum) of the two invading species and more detailed investigations could not confirm a causal relationship between the increasing invaders and decreasing mussel beds. There is evidence that the decline of mussel beds is mainly caused by failing spatfall possibly due to mild winters, whereas the increase in slipper limpets and oysters is facilitated by mild winters and warm summers, respectively. We conclude that changing species composition is a result of the climatic conditions in the last decade and that there is no evidence yet that the exotic species caused the decline of the natives. It remains an open question whether the species shift will continue and what the consequences for the native ecosystem will be.     

Gracilaria-Mytilus interaction on a commercial algal farm in Chile

Mytilus chilensis is an invertebrate that competes for space with the alga Gracilaria chilensis in farmed areas in Chile and, for this reason, is considered a contaminant organism. Mussel beds are considered to play a role in the regeneration of nitrogen and, as a consequence, they could be an important source of ammonium for the algae. In this study, we manipulated the mussel cover in experimental plots, creating replicated areas with 0%, 30% and 60% coverage. In half of the plots the mussels were killed with a gas torch so their effect would be mechanical, without nutrient regeneration. After 15 days, each plot was planted with 12 G. chilensis bundles (100 g each) per square meter. Ammonium concentrations increased significantly in the waters around the mussel bed in contrast to areas without mussels or dead mussels. Mussel cover had a significant negative effect on the length of the G. chilensis bundles planted in the experimental plots. However, no significant differences were detected between experimental quadrats with live mussels and those with dead mussels during a 5 month period. These results indicate that the mechanical effect of the mussel can, to some extent, be responsible for the decline in G. chilensis abundance in farms where mussel beds have been established.     

Relationship between the aerobic and anaerobic metabolic capacities and the vertical distribution of three intertidal sessile invertebrates: Jehlius cirratus(Darwin) (Cirripedia), Perumytilus purpuratus (Lamarck) (Bivalvia) and Mytilus chilensis (Hupé) (Bivalvia)

In protected areas of the southern Chilean coastline, the barnacle Jehlius cirratus dominates the upper intertidal zone, the bivalve Perumytilus purpuratus is the dominating species in the intermediate zone and Mytilus chilensis in the middle-lower zone. Varying degrees of aerial respiration were observed in the laboratory for these three sessile invertebrates: 80–100% of the immersed oxygen uptake for Jehlius cirratus, 30–50% for Perumytilus purpuratus and 5–15% for Mytilus chilensis. The pyruvate kinase/phosphoenolpyruvate carboxykinase (PK/PEPCK) ratio (adductor muscle) was higher for P. purpuratus than for M. chilensis. J. cirratus had no PEPCK activity in total soft tissues, under the assay conditions used in this study, and PK activity was higher for the cirriped than that of both bivalves. Succinate was produced in both mussels when exposed to hypoxic conditions, but it was not detected in J. cirratus. The kinetic parameters of the PK revealed that M. chilensis presented the highest _0.5 value for PEP and J. cirratus the lowest. Alanine inhibited the PK from M. chilensis to a greater extent (higher n_H value) and did not affect the PK of the cirriped. This latter enzyme also presented a marked substrate inhibition, above PEP concentrations of 0.5 mM. The evidence suggests that organisms inhabiting the upper intertidal zone could utilize an aerobic metabolism, given their high aerial respiration capacity, and that the succinate anaerobic pathway could be a more important metabolic strategy in species of the middle-lower intertidal zone. The physiological and biochemical capacities of these three species could thus be correlated with their vertical distribution in the intertidal rocky shore.     

Genetic Divergence Detected by ISSR Markers and Characterization of Microsatellite Regions in Mytilus Mussels

The wide distribution of microsatellites in mussels of the Mytilus edulis complex (Mytilidae) enables the analysis of inter-simple-sequence repeat (ISSR) markers. The aim of this investigation was to assess genetic differentiation in six sampling localities distributed along the European Atlantic coast to expose the potential of these markers in genetic studies requiring the detection of low polymorphism and as a source of sequences for developing microsatellite markers. We detected low genetic structuring within each member of the Mytilus edulis complex. Nei and Li distances and AMOVA clustered the individuals studied into two groups. On the basis of these results two sampling localities coming from the M. edulis × M. galloprovincialis mosaic hybrid zone in Western Europe were assigned to one species. On the other hand, mussels of a sampling locality in the Baltic Sea were not significantly different from a pure M. edulis locality supporting an extensive introgression of M. edulis in these individuals. Finally, 148 microsatellites were found in the sequences of 51 ISSR markers, and two polymorphic microsatellite markers were developed.     

ASYMMETRIC INTROGRESSION OF MITOCHONDRIAL DNA AMONG EUROPEAN POPULATIONS OF BLUE MUSSELS (MYTILUS SPP.)

Abstract.—Mytilus edulis and M. galloprovincialis are two blue mussel species that coexist in western Europe. Previously, we reported that M. galloprovincialis populations contain female and male haplotypes that are fixed in M. edulis populations as well as unique haplotypes. This study assesses whether paraphyly for these species is due to introgression or incomplete lineage extinction. The lineage extinction hypothesis predicts that the shared mtDNA haplotypes in M. galloprovincialis will be significantly diverged from those in M. edulis and form distinct sequence clades. In contrast, the introgression hypothesis proposes that M. edulis haplotypes have only recently been introduced into M. galloprovincialis through hybridization with relatively little divergence accumulating between the shared RFLP haplotypes. We examined 80 mtl6S gene sequences for both the maternal and paternal mtDNA lineages from mussels sampled from various European populations and found strong support for the introgression hypothesis. In addition, we found that M. edulis mtDNA haplotypes appear to be introgressing into mussel populations in the Baltic Sea, which have predominantly M. trossulus nuclear genotypes, indicating that introgressive hybridization is prevalent among European mussel populations.     

Changes in trace metal concentrations in the tissues of the White Sea mussel <Emphasis Type="Italic">Mytilus edulis</Emphasis> over the reproductive cycle

Seasonal changes in the concentrations and total amounts (contents) of Cd, Zn, and Cu in the mussel Mytilus edulis cultivated in the White Sea were studied over the reproductive cycle (prespawning, spawning, and postspawning stages). The results, when compared with published data on the closely related species M. trossulus from the Sea of Japan, suggest that the seasonal dynamics of trace element contents in mussel tissues are related to specific geochemical conditions, as well as to the dynamics of changes in soft tissue weight over the reproductive cycle. The contents of Cd and Cu in the mussels before, during, and after spawning changed similarly in the mollusks from the White Sea and the Sea of Japan. Changes in the Zn content at different stages of the reproductive cycle of the White Sea mussels were similar to those in mussels from the Sea of Japan but had smaller amplitude. The concentration of Zn in the White Sea mussels was before spawning the highest, but still lower than in mussels from the Sea of Japan. After the spawning, the Zn concentration in the White Sea mussels, in contrast to the Pacific mussels, decreased because of the redistribution of this element during the prespawning period from the somatic tissue into the gonad.     

Selective settlement of the barnacle Semibalanus balanoides (L.) facilitates its growth and reproduction on mussel beds in the Wadden Sea

On the unstable sedimentary tidal flats of the Wadden Sea, a suitable attachment substrate for sessile organisms is generally lacking. Epibenthic mussel beds (Mytilus edulis L.) provide the only and strongly limited settlement sites available for the barnacle, Semibalanus balanoides (L.). Field investigations showed that barnacles were non-randomly distributed within a mussel bed. They preferentially occurred near the siphonal apertures of living mussels but rarely grew on dead mussels or shell fragments. Field experiments revealed that this was due to selective settlement of barnacle cyprid larvae. Growth of barnacles was significantly higher upon living mussels than on empty mussel shells. Moreover, a higher reproductive output was obtained by individuals on living mussels which produced twice as many nauplii larvae than barnacles attached to empty shells. This study shows that selective settlement of S. balanoides cyprid larvae on living mussels is adaptive with respect to individual fitness. Received in revised form: 15 January 2001 Electronic Publication     

Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile,and considerations on the functional role of mussel beds

The fauna associated with hard bottom mussel beds along the exposed Pacific coast of Chile was examined. The abundance of adult (>10 mm body length) purple mussels Perumytilus purpuratus varied between 32 and 75 individuals per 50 cm², and their biomass between 4.8 and 8.6 g AFDW per 50 cm² at eight sampling sites between Arica (18°S) and Chiloé (42°S). At all sampling sites, the associated fauna was dominated by suspension-feeding organisms (cirripeds, spionid and sabellid polychaetes, a small bivalve) followed by grazing peracarids and gastropods. Predators and scavengers also reached high abundances while deposit- and detritus-feeding organisms were of minor importance. The majority of organisms associated with these hard bottom mussel beds feed on resources obtained from the water column or growing on the mussels rather than on materials deposited by the mussels. This is in contrast to the fauna associated with mussel beds on soft bottoms, which comprises many species feeding on material accumulated by mussels (faeces and pseudofaeces) and deposited within the mussel bed. Many of the organisms dwelling between mussels both on hard bottoms and on soft bottoms have direct development, but organisms with pelagic development also occur abundantly within mussel beds. We propose that species with direct development are disproportionately favoured by the structurally complex habitat with diverse interstitial spaces between the mussels, which provides ample shelter for small organisms. We conclude that mussels on hard-bottoms primarily provide substratum for associated fauna while mussels on soft bottoms provide both substratum and food resources. Electronic Publication     

The Influence of Salinity on Early Ontogeny of the Mussel Mytilus edulisand the Starfish Asterias rubensfrom the White Sea

The influence of increased and decreased salinity on early larvae of the mussel Mytilus edulisL. and the starfish Asterias rubensfrom the White Sea is studied. Fertilized egg cells, embryos, larvae, and yearlings of the two species were compared. Salinity tolerance changes with the stage of development of mussels and starfish. Morphological changes occurring in eggs and embryos exposed to extremely high and low salinities are reported.     

Benefit from an invader: American slipper limpet <Emphasis Type="Italic">Crepidula fornicata</Emphasis>reduces star fish predation on basibiont European mussels

Introduced species have recently become a major concern in ecological research and aquatic conservation. This is due to an increasing appearance of introduced species at a global scale and a multitude of negative impacts on native biota. However, impacts of introduced species are not necessarily only negative. The epizootic American slipper limpet Crepidula fornicata, native at North American Atlantic shores, was introduced to Europe in the 1870s and is now widespread along the Atlantic coast of Europe. Negative effects like trophic and spatial competition have been reported. In its major basibiont in the Wadden Sea, the blue mussel Mytilus edulis, attached limpets reduce survival and growth. However, a laboratory experiment also showed sea star (Asterias rubens) predation on mussels with limpet epigrowth to be three times lower than in unfouled mussels. Hence, although negatively affected by C. fornicatain one way, this epigrowth is beneficial for fouled mussels in another. This indicates that the actual impact of an introduced species is a complex interplay of positive and negative effects which may only be revealed experimentally.     

The site of settlement indicates commensalism between bluemussel and its epibiont

Summary The site of settlement of barnacles (Balanus improvisus) attached on shells of bluemussels (Mytilus edulis) was mapped from a sample of mussels collected in the Baltic Sea. Most barnacles had settled near the siphonal apertures of the mussel. An experiment was made to measure the disadvantages and advantages that living in close association brings to barnacles and mussels. The barnacles on shells of living mussels were shown to grow significantly faster than those on empty mussel shells. Presence of barnacles had no effects on growth of mussels. The two-species association under study was demonstrated to be a case of commensalism.     

The American slipper limpet <Emphasis Type="Italic">Crepidula fornicata </Emphasis>(L.) in the northern Wadden Sea 70 years after its introduction

In 1934 the American slipper limpet Crepidula fornicata (L.) was first recorded in the northern Wadden Sea in the Sylt-R?m? basin, presumably imported with Dutch oysters in the preceding years. The present account is the first investigation of the Crepidula population since its early spread on the former oyster beds was studied in 1948. A field survey in 2000 revealed the greatest abundance of Crepidula in the intertidal/subtidal transition zone on mussel (Mytilus edulis) beds. Here, average abundance and biomass was 141 m^–2 and 30 g organic dry weight per square metre, respectively. On tidal flats with regular and extended periods of emersion as well as in the subtidal with swift currents in the gullies, Crepidula abundance was low. The main substrate of attachment was live mussels. Compared with the years following their initial introduction, Crepidula is more abundant today and has shifted from the now extinct oyster beds to the epifaunal community of the mussel beds. Their present abundance is considerably lower than at more southern European coasts where the species may dominate the epifauna. Low winter temperatures are suggested to have limited the population expansion in the northern Wadden Sea until now. Electronic Publication     

On the dynamics of the stocks of blue mussels (Mytilus edulis L.) in the Danish Wadden Sea

As biological basis for the monitoring programme for the commercially exploited stock(s) of mussels (Mytilus edulis L.) in the Danish Wadden Sea, samples of mussels have been collected regularly since 1986, both from sub-tidal and inter-tidal mussel beds. These samples are the basis for the estimation of total biomass. They also provide data on size frequency distributions, which have been analysed for cohort identification resulting in length at age data, which again have been used for estimating parameters (L and K) for the von Bertalanffy growth equation (VBGE) as well as mortality parameters. By applying these in the Beverton & Holt model, estimates of average biomass and annual production (P) of the mussels have been obtained together with possible fisheries yields from the beds. The growth and mortality parameters and the figures for annual production and P/B are compared with figures from other investigations. These analyses have been the basis for annual assessments of the mussel stocks, which again are used in the current management of mussel fishery in the Danish Wadden Sea.     

Differential effects of the severe winter of 1995/96 on the intertidal bivalves Mytilus edulis, Cerastoderma edule and Mya arenaria in the Northern Wadden Sea

Intertidal mussel beds were severely damaged by scouring ice floes during the winter of 1995/96. Aerial surveys before and after the winter showed that more clusters of mussel beds vanished in a region with a higher areal share of tidal flats and a lower salinity, suggesting that the amount of ice present determined the magnitude of the disturbance on beds of Mytilus edulis. Nehls and Thiel [(1993) Neth J Sea Res 31:181–187] observed a strikingly similar spatial pattern of disturbances caused by severe storms in the Wadden Sea. Areas on mussel beds mechanically undisturbed by ice showed no reduced abundance and biomass of mussels, indicating that temperature alone was of little importance as a lethal factor. Conversely, Cerastoderma edule was strongly affected by low temperature. On average 80% died during the winter with extinctions up to 100% in the high tidal zone. At the lowest tidal level, surviving cockles were larger than those killed by the frost. A reinvestigation of sampled sites in autumn revealed that substantial further mortality had occurred during spring and summer which may constitute a time-lag effect of the preceding winter. There was no increased mortality in juvenile and adult Mya arenaria during the winter of 1995/96, confirming that this clam is a hard-winter species like Macoma balthica. Received in revised form: 7 May 2001 Electronic Publication     

Hierarchical spatial structure in soft-bottom mussel beds

Mussels (Mytilus edulis L.) are unusual because they thrive in both rocky shore and soft-bottom habitats. Despite their ecological and economic importance, little is known about their spatial structure. Mussels do not generally recruit to bare soft substrate because larvae and postlarvae cannot attach to a bottom of small sediment particles. They attach to hard objects on the sediment surface (especially other mussels), so soft-bottom mussel beds may be spatially organized in ways that are fundamentally different from those on rocky shores. The purpose of our study was to characterize the scales of spatial variability for several mussel abundance parameters in soft-bottom, intertidal M. edulis beds in coastal Maine. We used a random factor nested-ANOVA design of 200 cm² Cores within 1 m² Quadrats within 6 m Transects within Positions within bed Sites along 70 km (euclidean distance) of the Maine coast. Based on the literature and our field observations, we hypothesized that Sites and Positions account for most of the spatial variance in soft-botttom mussel beds. We rejected this hypothesis. Sites and Positions were not important in explaining variation in total mussel density, density of new recruits, or density of larger mussels. Although most of the variance in surface silt-clay fraction did occur at these levels, most mussel variation occurred at smaller spatial scales, specifically at the Quadrat scale for new recruits and total mussels and at the Transect scale for larger mussels. Variance in mussel parameters was not closely linked to the silt-clay fraction of surface sediment or to Site rankings of wind exposure and tidal flow. Variance in total mussel density was due primarily to variance in recruitment. No single scale explained more than about half the mussel variance, and no single scale was best at explaining all the mussel parameters. Greater knowledge about mussel bed spatial variability would be useful because it can help direct scale-dependent sampling regimes, field experiments, and coastal management practices.     

Effects ofFucus vesiculosus covering intertidal mussel beds in the Wadden Sea

The brown algaFucus vesiculosus formamytili (Nienburg) Nienhuis covered about 70% of mussel bed (Mytilus edulis) surface area in the lower intertidal zone of Königshafen, a sheltered sandy bay near the island of Sylt in the North Sea. Mean biomass in dense patches was 584 g ash-free dry weight m^?2 in summer. On experimental mussel beds, fucoid cover enhanced mud accumulation and decreased mussel density. The position of mussels underneath algal canopy was mainly endobenthic (87% of mussels with >1/3 of shell sunk into mud). In the absence of fucoids, mussels generated epibenthic garlands (81% of mussels with <1/3 of shell buried in mud). Mussel density underneath fucoid cover was 40 to 73% of mussel density without algae. On natural beds, barnacles (Balanidae), periwinkles (Littorina littorea) and crabs (particularly juveniles ofCarcinus maenas) were significantly less abundant in the presence of fucoids, presumably because most of the mussels were covered with sediment, whereas in the absence of fucoids, epibenthic mussel clumps provided substratum as well as interstitial hiding places. The endobenthic macrofauna showed little difference between covered and uncovered mussel beds. On the other hand, grazing herbivores — the flat periwinkleLittorina mariae, the isopodJaera albifrons and the amphipodsGammarus spp. — were more abundant at equivalent sites with fucoid cover. The patchy growth ofFucus vesiculosus on mussel beds in the intertidal Wadden Sea affects mussels and their epibionts negatively, but supports various herbivores and increases overall benthic diversity.