Morphology of the Bivalve Mollusks Crenomytilus grayanus and Mytilus coruscus in Relation to Their Spatial Distribution in the Upper Subtidal Zone

The morphology of the shell and byssus threads was studied in two closely related mussel species Crenomytilus grayanus and Mytilus coruscus. The two species differ significantly from each other in the shell shape and in the degrees of development and deformation of byssus threads. These differences, in turn, determine (either directly or indirectly) the differences in strength of the byssal attachment and are discussed in terms of their functional morphology with respect to the spatial distribution of the mussels in marine coastal zones.     

Dynamics of byssal thread production in <Emphasis Type="Italic">Crenomytilus grayanus</Emphasis> and <Emphasis Type="Italic">Modiolus modiolus</Emphasis> (Bivalvia) upon reattachment to substrate

It was established that the process of repeated attachment to a substrate in bivalve mollusks Crenomytilus grayanus (Grays mussel) and Modiolus modiolus (the northern horse mussel) involved several successive stages which took in vitro about one month at a water temperature of 19 ± 2°C. Comparison with Grays mussel revealed that the northern horse mussel had a higher rate of byssal thread production and a greater thread number by the end of the complete formation of the byssus complex. The observed differences are explained by the adaptation of mollusks to habitation in different biotopes.Original Russian Text Copyright © 2004 by Biologiya Morya, Selin, Vekhova.     

Effect of the excretory-secretory products of some marine invertebrates on byssus production of the blue mussel <Emphasis Type="Italic">Mytilus edulis</Emphasis> (Bivalvia: Mytilidae)

Under laboratory conditions, we investigated byssus production in the blue mussel Mytilus edulis, as affected by the excretory-secretory products (ESPs) of the mussel itself and some marine invertebrates: the predatory starfish Asterias rubens, and organisms competing with mussels in White Sea fouling communities—a bivalve Hiatella arctica, the solitary ascidians Styela rustica and Molgula citrine, and a sponge Halichondria panicea. The number of attachment disks produced by a mussel per day and the thickness of byssal threads were estimated. Excretory-secretory products of H. arctica and M. citrine had no effect on the number of attachment disks, while ESPs of S. rustica, H. panacea and A. rubens stimulated mussels to produce attachment plaques. The activity of the mussel was slightly increased at low levels of its own ESPs in seawater. The thickness of byssal threads decreased with an increase in the ESPs of mussels in seawater, but it increased in experiments with the ESPs of any other species tested.     

Byssal proteins of the freshwater zebra mussel,Dreissena polymorpha

The freshwater zebra mussel (Dreissena polymorpha) is a notorious biofouling organism. It adheres to a variety of substrata underwater by means of a proteinaceous structure called the byssus, which consists of a number of threads with adhesive plaques at the tips. The byssal proteins are difficult to characterize due to extensive cross-linking of 3,4-dihydroxyphenylalanine (DOPA), which renders the mature structure largely resistant to protein extraction and immunolocalization. By inducing secretion of fresh threads and plaques in which cross-linking is minimized, three novel zebra mussel byssal proteins were identified following extraction and separation by gel electrophoresis. Peptide fragment fingerprinting was used to match tryptic digests of several gel bands against a cDNA library of genes expressed uniquely in the mussel foot, the organ which secretes the byssus. This allowed identification of a more complete sequence of Dpfp2 (D. polymorpha foot protein 2), a known DOPA-containing byssal protein, and a partial sequence of Dpfp5, a novel protein with several typical characteristics of mussel adhesive proteins.     

Assessment of the adaptation capabilities of the bivalves Modiolus modiolus (Linnaeus, 1758) and Crenomytilus grayanus (Dunker, 1853) under increased levels of heavy metals in the environment

The active biomonitoring method was used to examine the changes in heavy-metal (Fe, Zn, Cu, Cd, Mn, Pb, and Ni) contents in the organs (muscle, gonads, mantle, gills, digestive gland, and kidney) of the mussels Crenomytilus grayanus and Modiolus modiolus. The dynamics of trace element concentrations in mussel organs during the experiment were compared with their subcellular distribution. The defense strategy of M. modiolus consisted of the threshold accumulation of toxic metals in all organs followed by their excretion, whereas the strategy of C. grayanus involved short-term isolation from adverse environmental influence. Under chronic pollution, in C. grayanus the main loads occurred in the digestive gland and kidney. Under acute changes in environmental conditions, the processes of regulation (detoxification/excretion) of Fe, Mn, and Pb in this species were impaired substantially.     

Comparative Analysis of Subcellular Distribution of Heavy Metals in Organs of the Bivalve Mollusks <Emphasis Type="Italic">Crenomytilus grayanus</Emphasis> and <Emphasis Type="Italic">Modiolus modiolus</Emphasis> in a Continuously Polluted Environment

The distribution of Zn, Fe, Ni, Cu, Mn, Cd, and Pb in subcellular fractions, and of Cd, Zn, and Cu in cytoplasm proteins of the kidney and digestive gland of the mussels Crenomytilus grayanus and Modiolus modiolus, sampled from contaminated and conditionally clean areas, was studied. It was found that, in a contaminated environment, the organs of mussels were more highly enriched with metals. It was shown that essential trace elements were accumulated mostly in the cytosol of organs of both molluscan species from contaminated areas, whereas in the background areas the trace elements were associated mostly with membrane structures in Gray's mussel, C. grayanus, and with the cytosol in M. modiolus, the northern horse mussel. The lead was bound mostly to membrane structures in organs of both mussel species at all stations. The method of gel chromatography enabled us to isolate metallothionein-like proteins from the kidney of the northern horse mussel sampled in contaminated areas, whereas their concentration in the kidney of Gray's mussels was lower than the limiting error of the method. It is supposed that in the kidney of Gray's mussel the synthesis of metallothionein-like proteins was quenched by the integrated effect of the accumulated metals.     

Facilitation and competition between invasive and indigenous mussels over a gradient of physical stress

The interactions between invasive exotic and indigenous species can have profound harmful effects on the recipient community; however, not all such interactions are negative. Facilitation is increasingly recognised as important in shaping natural communities and is believed to vary under different conditions. Earlier studies have shown that the indigenous intertidal mussel Perna perna initially facilitates survival of the invasive Mytilus galloprovincialis in the low mussel zone by providing protection against waves, but later excludes M. galloprovincialis through interference competition for space. Here, we examined interactions between these species in the mid and upper mussel zones, moving mussels to experimental plots in different combinations of densities and species. Mussels were left on the shore for more than a year and treatment effects on mortality, shell length and condition were compared. In the high zone, treatment had no effects and P. perna showed greater mortality than M. galloprovincialis, indicating that its exclusion from the high shore is due to emersion stress. In the mid zone, treatment had no significant effects on M. galloprovincialis, but multiple comparisons among treatments involving P. perna showed that facilitation occurred. P. perna survived better at higher densities, but survived even better when mixed with the physiologically more tolerant M. galloprovincialis. Length data indicated both inter- and intraspecific competition for P. perna in the mid zone. Whereas facilitation occurs strongly in the low zone (P. perna facilitates M. galloprovincialis) and weakly in the mid zone (M. galloprovincialis facilitates P. perna), the lack of facilitation in the high zone suggests that the probability of facilitation is not linearly linked to increasing physical stress. Instead it is likely to be hump shaped: relatively unimportant under conditions that are benign for a particular species, significant under more severe conditions, and overridden by physical stress under very harsh conditions.     

Novel Proteins Identified in the Insoluble Byssal Matrix of the Freshwater Zebra Mussel

The freshwater zebra mussel, Dreissena polymorpha, is an invasive, biofouling species that adheres to a variety of substrates underwater, using a proteinaceous anchor called the byssus. The byssus consists of a number of threads with adhesive plaques at the tips. It contains the unusual amino acid 3, 4-dihydroxyphenylalanine (DOPA), which is believed to play an important role in adhesion, in addition to providing structural integrity to the byssus through cross-linking. Extensive DOPA cross-linking, however, renders the zebra mussel byssus highly resistant to protein extraction, and therefore limits byssal protein identification. We report here on the identification of seven novel byssal proteins in the insoluble byssal matrix following protein extraction from induced, freshly secreted byssal threads with minimal cross-linking. These proteins were identified by LC-MS/MS analysis of tryptic digests of the matrix proteins by spectrum matching against a zebra mussel cDNA library of genes unique to the mussel foot, the organ that secretes the byssus. All seven proteins were present in both the plaque and thread. Comparisons of the protein sequences revealed common features of zebra mussel byssal proteins, and several recurring sequence motifs. Although their sequences are unique, many of the proteins display similarities to marine mussel byssal proteins, as well as to adhesive and structural proteins from other species. The large expansion of the byssal proteome reported here represents an important step towards understanding zebra mussel adhesion.     

Growth and shell morphology of three mytilidae (Bivalvia) species from the Sea of Japan

The growth and shell morphology of bivalve mollusks Crenomytilus grayanus, Mytilus coruscus, and Modiolus modiolus from the Sea of Japan are examined. The changes in body proportions and shell form in the ontogenesis of C. grayanus, M. coruscus, and M. modiolus are different even in the cases when the mussels develop in similar environmental conditions. Rapid growth shapes a well-streamlined and flat form of shell; slow growth leads to the formation of a massive and convex form. The parameters of the Bertalanffy growth curve for each species are calculated. The differences are discussed from the standpoint of functional morphology and spatial distribution patterns of mytilids in the coastal areas of the sea.     

Spatial distribution of proteins in the quagga mussel adhesive apparatus

The invasive freshwater mollusc Dreissena bugensis (quagga mussel) sticks to underwater surfaces via a proteinacious ‘anchor’ (byssus), consisting of a series of threads linked to adhesive plaques. This adhesion results in the biofouling of crucial underwater industry infrastructure, yet little is known about the proteins responsible for the adhesion. Here the identification of byssal proteins extracted from freshly secreted byssal material is described. Several new byssal proteins were observed by gel electrophoresis. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry was used to characterize proteins in different regions of the byssus, particularly those localized to the adhesive interface. Byssal plaques and threads contain in common a range of low molecular weight proteins, while several proteins with higher mass were observed only in the plaque. At the adhesive interface, a plaque-specific ~8.1 kDa protein had a relative increase in signal intensity compared to the bulk of the plaque, suggesting it may play a direct role in adhesion.     

Antifoulant diterpenes produced by the brown seaweed Canistrocarpus cervicornis

This paper reports the antifouling properties of the dichloromethane crude extract (DC) and 3 pure compounds isolated from the Brazilian brown seaweed Canistrocarpus cervicornis against establishment of the mussel Perna perna. DC extract showed a strong inhibition activity against byssal threads. Two natural dolastanes and one seco-dolastane diterpene, namely (4R, 9S, 14S)-4α-acetoxy-9β,14α-dihydroxydolast-1(15),7-diene (1), (4R,7R,14S)-4α,7α-diacetoxy-14-hydroxydolast-1(15),8-diene (2) and isolinearol (3), were isolated from DC extract. Dolastane (1) inhibited 60% of byssal fixation, while compound 2 and the seco-dolastane (3) strongly inhibited (82%) the establishment of P. perna. This is the first report of this type of chemical skeleton in three powerful compounds that could be further explored for the development of antifouling technology.     

Use of the photo method in the study of the composition and abundance of soft-bottom macrobenthos

The composition and abundance of the macrobenthic fauna associated with soft-bottom beds of the large bivalve mollusks Crenomytilus grayanus and Modiolus modiolus were studied in the inner part of Vostok Bay (Sea of Japan) in spring 2010. More than 30 taxa of animals were found in the mussel beds. Comparison of the data obtained with three different methods of studying muddy-bottom mussel communities showed that 80% of their biomass and only up to 25% of the species composition and 19% of the abundance can be estimated by the photo method. Photo surveys disregard small and/or juvenile animals, as well as infaunal organisms, and thus do not give a complete picture of the species, size, and age composition and abundance of biota.     

A comparative study of byssogenesis on zebra and quagga mussels: the effects of water temperature, salinity and light-dark cycle

The quagga mussel (Dreissena rostriformis bugensis) and zebra mussel (Dreissena polymorpha) are invasive freshwater bivalves in Europe and North America. The distribution range of both Dreissena species is still expanding and both species cause major biofouling and ecological effects, in particular when they invade new areas. In order to assess the effect of temperature, salinity and light on the initial byssogenesis of both species, 24 h re-attachment experiments in standing water were conducted. At a water temperature of 25°C and a salinity of 0.2 psu, the rate of byssogenesis of D. polymorpha was significantly higher than that of D. rostriformis bugensis. In addition, byssal thread production by the latter levelled out between 15°C and 25°C. The rate of byssogenesis at temperatures<25°C was similar for both species. Neither species produced any byssal threads at salinities of 4 psu or higher. At a salinity of 1 psu and a water temperature of 15°C, D. polymorpha produced significantly more byssal threads than D. rostriformis bugensis. There was no significant effect of the length of illumination on the byssogenesis of either species. Overall, D. polymorpha produced slightly more byssal threads than D. rostriformis bugensis at almost all experimental conditions in 24 h re-attachment experiments, but both species had essentially similar initial re-attachment abilities. The data imply that D. rostriformis bugensis causes biofouling problems identical to those of D. polymorpha.     

Mechanisms of successional dynamics: Consumers and the rise and fall of species dominance

Insight into potential mechanisms of succession following disturbance to an ecological community can be gained by considering processes that contribute to the rise (colonization, interactions with established species) and demise (differential mortality) of specific stages within the successional sequence. Most successional theories focus on the rise to dominance, assuming demise is the result of competition, but other factors can cause differential mortality among species, including physical disturbance, senescence, and consumers. In rocky intertidal communities on the coast of Washington state, USA, gaps in mussel beds exhibit a succession from predator-susceptible to predator-resistant species following disturbance, suggesting that differential consumption by mobile species may play an important role in the demise of early succession species and the eventual dominance of the mussel Mytilus californianus. Experimental manipulation of a dominant species earlier in succession, the blue mussel Mytilus trossulus, demonstrated that this species inhibits the invasion of M. californianus in the absence of predators. Experimental manipulation of predatory snails (Nucella emarginata and Nucella canaliculata), which feed heavily on M. trossulus but not M. californianus, greatly increased the rate at which M. californianus invaded gaps. These results and those of other studies indicate that consumers frequently have important effects on the dynamics of succession in benthic marine systems, and might also play a role in other settings.     

The glue protein of ribbed mussels (Geukensia demissa): a natural adhesive with some features of collagen

Summary The Atlantic ribbed musselGeukensia (Modiolus)demissa attaches itself to the roots of cord grass and other hard objects in tidal salt marshes by spinning adhesive byssal threads. The precursor of a protein apparently present in the adhesive plaques of the threads was isolated in quantity from the foot of the mussel. The protein has an apparent molecular weight of 130000, a pI of 8.1, and contains a high proportion of Gly, Glu/Gln, Lys and 3,4-dihydroxyphenyl-l-alanine (DOPA). Sequence of tryptic peptides suggests a pattern of repeated motifs, such as: Gly-DOPA-Lys, and X-Gly-DOPA-Y-Z-Gly-DOPA/Tyr-Lys, where X is Thr or Ala in octapeptides and Gln-Thr in nonapeptides. Y is variable, but more often than not hydrophobic; and Z is frequently Pro or 4-trans-hydroxyproline (Hyp). The presence of Pro-Gly and Hyp-Gly sequences of -hydroxylysine in the protein is reminiscent of typical collagens; however, the protein is not labile to clostridial collagenase, nor does collagen cross-react with antibodies raised against the mussel protein. Unlike typical collagens, Gly probably occurs only at every 4th or 5th residue in this unusual mussel protein.Abbreviations Anti-Gdfp anti-G. demissa foot protein - Dopa 3,4-dihydroxyphenylalanine - CTAB cetyltrimethylammonium bromide - HPLC high performance liquid chromatography - PAGE polyacrylamide gel electrophoresis Supported by grants from the National Science Foundation (DMB 8500301) and the Office of Naval Research (N00014-86K-0717)     

Attachment strength of an adhesive nuisance mussel,limnoperna fortunei,against water flow

The attachment strength of the freshwater mussel Limnoperna fortunei against water flow was studied. Newton's expression successfully described the hydrodynamic drag force acting on the mussel with a drag coefficient value of 1.03. The drag‐resistant force (defined as hydrodynamic drag force at mussel detachment) was smaller than the detachment force measured using a tensile load test. A fairly good correlation was obtained between the drag‐resistant force and the number of secreted threads. The drag‐resistant force divided by the number of threads increased with shell size, suggesting that byssal thread strength increased with mussel growth. For the mussel specimens obtained from a water transmission pipe, thread width increased with shell size. However, thread width was not dependent on current velocity. There was no correlation between the number of secreted threads and shell length, which indicated that the number of secreted threads did not change with mussel size. Therefore, the water velocity needed to detach mussels increases with shell size of the mussel when the number of secreted threads is constant. The increases in the water velocity to detach mussels with larger shells suggests that the mussel becomes more resistant to water flow as it grows. It is estimated that a flow velocity of around lms^‐1 is critical for attachment/detachment of a juvenile mussel with a shell length of a few millimeters and one hundred byssal threads.     

Byssus production rate of the White Sea blue mussel <Emphasis Type="Italic">Mytilus edulis</Emphasis> (Linnaeus, 1758) in the presence of metabolites of some hydrobionts

The byssus production of the blue mussel Mytilus edulis L. was studied in the laboratory in the presence of the metabolites of the following animals: a predator (a starfish Asterias rubens L.) and several species competing with the mussel in White Sea fouling communities (a bivalve Hiatella arctica L. and a solitary ascidian Styela rustica L.). The byssus threads and attachment plaques produced by each mussel per day were counted. The number of byssus threads and plaques was smallest in pure sea water and in the presence of metabolites produced by conspecific individuals.     

Filamentous Fungi Associated with Bivalve Mollusks from Polluted Biotopes of Ussuriiskii Bay,Sea of Japan

We have studied for the first time the taxonomic composition of filamentous fungi associated with the bivalve mollusks Crenomytilus grayanus (Bunker, 1853) and Modiolus modiolus (Linnaeus, 1758), collected in polluted biotopes of Ussuriiskii Bay (Peter the Great Bay, Sea of Japan). One hundred fifty-five strains of higher fungi were isolated, and 35 species of filamentous fungi were identified. Out of these, 28 species were anamorphous fungi of the genera Aspergillus (12), Penicillium (10), Acremonium (1), Alternaria (1), Aureobasidium (1), and Cladosporium (3) (Deuteromycota), and 7 were species of the genera Chaetomium (6) and Myxotrichum (1) (Ascomycota). Twenty-four species of filamentous fungi were isolated from the internal organs of C. grayanus: 8 from the muscles, 8 from the hepatopancreas, 6 from the female gonads, 4 from the mantle, 3 from the kidneys and male gonads, and 1 from the gills. Twenty-one species of filamentous fungi were isolated from the internal organs of Modiolus modiolus: 10 from the muscles, 6 from the hepatopancreas, 5 from the female gonads, 3 from the kidneys, 3 from the mantle, and 1 from the gills. The bulk of the isolated species of the genera Aspergillus, Penicillium, Cladosporium, and Chaetomium were pathogenic and toxigenic fungi.     

Proteomic approach to probe for larval proteins of the mussel Mytilus galloprovincialis

A proteomic approach was used to search for larval proteins specific to the mussel Mytilus galloprovincialis from Galicia in northwest Spain. The study included both a comparative analysis, through two-dimensional electrophoresis, of protein expression maps of the larvae of the mussel and of 5 abundant and commercially important bivalve species from the region (Ostrea edulis, Cerastoderma edule, Pecten maximus, Tapes decussatus, and Venarupis pullastra) and subsequent mass spectrometric analysis of some of the protein spots. A total of 18 spots were selected and isolated from gels of M. galloprovincialis larvae. From their relative position on the electrophoresis gels, 6 of these were clearly exclusive to the mussel species. However, it was not clear whether the other spots were shared by other species. To overcome this ambiguity, first an analysis using matrix assisted laser desorption ionization with time-of-flight (MALDI-TOF) was conducted on the 6 spots of Mytilus that could possibly be shared with only one species. The peptide mass fingerprinting was completely different for the proteins compared. This result confirmed that the 6 proteins were exclusively mussel proteins, but demonstrated the utility of this approach when working with species that are poorly represented at the protein level in databases.     

Photosynthetic characteristics and mycosporine-like amino acids under UV radiation: a competitive advantage of Mastocarpus stellatus over Chondrus crispus at the Helgoland shoreline?

Chondrus crispus and Mastocarpus stellatus both inhabit the intertidal and upper sublittoral zone of Helgoland, but with C. crispus generally taking a lower position. Measurements of chlorophyll fluorescence, activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO), and content and composition of UV absorbing mycosporine-like amino acids (MAAs) were conducted in the laboratory, to test whether susceptibility to UV radiation may play a role in the vertical distribution of these two species. Effective and maximal quantum yield of photochemistry as well as maximal electron transport rate (ETR_max) in C. crispus were more strongly affected by UV-B radiation than in M. stellatus. In both species, no negative effects of the respective radiation conditions were found on total activity of RubisCO. Total MAA content in M. stellatus was up to 6-fold higher than in C. crispus and the composition of MAAs in the two species was different. The results indicate that, among others, UV-B sensitivity may be a factor restricting C. crispus to the lower intertidal and upper sublittoral zone, whereas M. stellatus is better adapted to UV radiation and is therefore more competitive in the upper intertidal zone. Received: 15 November 1999 / Received in revised form: 28 February 2000 / Accepted: 10 March 2000