Ecotoxicological impacts of exposure to copper oxide nanoparticles on the gill of the Swan mussel,Anodonta cygnea (Linnaeus, 1758)

This study was conducted to investigate the ecotoxicological effects of exposure to copper oxide nanoparticles (CuO NPs) on the gill of the swan mussel Anodonta cygnea using several approaches including qualitative and quantitative histopathology, ultra-morphology (scanning electron microscopy [SEM]) and measures of clearance rate (CR) and bioaccumulation of CuO NPs. Histological alterations in mussels exposed to 0.25 (T1), 2.5 (T2) and 25.0?µg L^?1 (T3) CuO NPs for 12 days include changes in the length and form of gill lamellae, changes in inter-lamellar spaces, epithelial hyperplasia, atrophy and tissue rupture. Ultra-morphological changes following CuO NP exposure included epithelial hyperplasia and hypertrophy, epithelial lifting, tissue rupture (water channel fusion) and extensive necrosis of the gill surfaces. I_Gill (gill damage severity) index values for both histopathological and ultra-morphological data were significantly (P?0.05) higher in T3. The CR of mussels was significantly (P??1 g^?1 dry weight]) in comparison to controls (CR?=?108?±?47.14 [L min^?1 g^?1 dry weight]). CuO NPs accumulated in exposed mussels at all exposure concentrations until day 4, but there was no further change in accumulation levels by the end of the exposure period. The accumulated content of CuO NPs was significantly (P??1 exposure concentration. Based on these results, significant accumulation of CuO NPs in the gills of swan mussel could affect histological and ultra-structural characteristics of this organ and consequently have deleterious impacts on its filtration activity.     

Impact of Engineered Zinc Oxide Nanoparticles on the Individual Performance of Mytilus galloprovincialis

The increased use of engineered nanoparticles (ENPs) in consumer products raises the concern of environmental release and subsequent impacts in natural communities. We tested for physiological and demographic impacts of ZnO, a prevalent metal oxide ENP, on the mussel Mytilus galloprovincialis. We exposed mussels of two size classes, <4.5 and ≥4.5 cm shell length, to 0.1–2 mg l⁻¹ ZnO ENPs in seawater for 12 wk, and measured the effect on mussel respiration, accumulation of Zn, growth, and survival. After 12 wk of exposure to ZnO ENPs, respiration rates of mussels increased with ZnO concentration. Mussels had up to three fold more Zn in tissues than control groups after 12 wk of exposure, but patterns of Zn accumulation varied with mussel size and Zn concentrations. Small mussels accumulated Zn 10 times faster than large mussels at 0.5 mg l⁻¹, while large mussels accumulated Zn four times faster than small mussels at 2 mg l⁻¹. Mussels exposed to 2 mg l⁻¹ ZnO grew 40% less than mussels in our control group for both size classes. Survival significantly decreased only in groups exposed to the highest ZnO concentration (2 mg l⁻¹) and was lower for small mussels than large. Our results indicate that ZnO ENPs are toxic to mussels but at levels unlikely to be reached in natural marine waters.     

The effect of chlorpyrifos on protein content and acid DNase activity in the mussel,Mytilus galloprovincialis

We evaluated the effects of short-term exposure to an organophosphate pesticide chlorpyrifos on the digestive gland and gills of the mussel Mytilus galloprovincialis. We studied metabolic activity by quantifying protein content and physiological function responses using acid DNase activity. The increase in protein content was observed in both the target tissues of mussels exposed to 0.03 μg/L chlorpyrifos when compared with control mussels. The pattern of acid DNase activity in digestive gland and gills indicated a tissue-specific response, although the lowest concentration of chlorpyrifos caused changes in acid DNase activity in both tissues. In the digestive gland, the increase of acid DNase activity was observed in mussel exposed to 0.03 μg/L chlorpyrifos, followed by decrease up to 100 μg/L chlorpyrifos. Enzyme activity in the gills showed a dose response effect. The results support the use of acid DNase activity in the digestive gland as a sensitive response to an environmentally relevant range of pesticide concentrations. It may also indicate an effect on mussel physiological status.     

Commensals of Mytilus galloprovincialis in the Black Sea: Urastoma cyprinae (Turbellaria) and Polydora ciliata (Polychaeta)

The intensity of infection of the mussel Mytilus galloprovincialis Lamarck in the Black Sea by the turbellarian Urastoma cyprinae (Graff), which lives on its gills, was found to be higher in larger hosts, reaching a maximum in mussels of 50–70 mm length. Greater numbers occured in mussels inhabiting a silty bottom than in cultivated mussels suspended above the bottom. Over the period 1982–1987, U. cyprinae was most numerous in winter and especially so in years that were colder. The spionid polychaete Polydora ciliata (Johnston) also infects M. galloprovincialis, burrowing into the shell. Young spionids of up to 1 mm length occured in mussels with a shell length of 35 mm. Numbers of this commensal reached a maximum in mussels of intermediate size.     

Changes of Blue Mussels Mytilus edulis L. Lipid Composition Under Cadmium and Copper Toxic Effect

The lipid and fatty acid composition of the blue mussels Mytilus edulis L. gills and digestive glands was evaluated after 24 and 72 h of cadmium (Cd) and copper (Cu) exposure. Mussels were exposed to different cadmium (10, 100, and 500 μg/L) and copper (5, 50, and 250 μg/L) concentrations. Similar stress response of predominant membrane phospholipids level as well as polyenoic and non-methylene interrupted (NMI) fatty acids content was observed in mussel gills under both cadmium and copper effects. Increased NMI fatty acids level after 24 h, the metal ions treatment suggests that these acids contribute to the protective response to the membrane oxidative stress caused by accumulation of the metals. The content of cholesterol, some minor membrane phospholipids, and storage lipids (triacylglycerols, TAG) in the mussels’ organs alter significantly under the cadmium and copper effect. A two-step response at the digestive glands TAG level depends on the duration of the cadmium and copper treatments (24 and 72 h) on the mussels. The results demonstrate that Cd and Cu impact has adverse effects on gills and digestive glands lipid and fatty acids composition. The type of observed effects varies with the nature and concentration of the metal ions and depends on the role of the metals in the mussels’ life activity.     

The influence of nutritional conditions on metal uptake by the mixotrophic dual symbiosis harboring vent mussel Bathymodiolus azoricus

The vent mussel Bathymodiolus azoricus, host thioautotrophic and methanotrophic bacteria, in their gills and complementary, is able to digest suspended organic matter. But the involvement of nutritional status in metal uptake and storage remains unclear. The influence of B. azoricus physiological condition on its response to the exposure of a mixture of metals in solution is addressed. Mussels from the Menez Gwen field were exposed to 50 μg L^− 1 Cd, plus 25 μg L^− 1 Cu and 100 μg L^− 1 Zn for 24 days. Four conditions were tested: (i) mussels harboring both bacteria but not feed, (ii) harboring only methanotrophic bacteria, (iii) without bacteria but fed during exposure and (iv) without bacteria during starvation. Unexposed mussels under the same conditions were used as controls. Eventual seasonal variations were assessed. Metal levels were quantified in subcellular fractions in gills and digestive gland. Metallothionein levels and condition indices were also quantified. Gill sections were used for fluorescence in situ hybridization (FISH) to assess the temporal distribution of symbiotic associations. Starvation damages metal homeostasis mechanisms and increase the intracellular Zn and MT levels function. There is a clear metallic competition for soluble and insoluble intracellular ligands at each condition. Seasonal variations were observed at metal uptake and storage.     

Comparative characteristics of the antioxidant glutathione complex in the black sea molluscs Mytilus galloprovincialis Lam. and Anadara inaequivalvis Br.

The peculiarities in distribution of lipid peroxidation (LPO) products, glutathione (GSH) level, and antioxidant enzymes-glutathione peroxidase (GP) and glutathione reductase (GR)—were studied in tissues of Black Sea bivalve molluscs, Anadata inaequivalvis Br. (anadara) and Mytilus galloprovincialis Lam. (mussel, black morph), as well as their comparative characteristics were presented. The differences were established in organization of the glutathione anti-oxidant system and the LPO intensity in tissues of these mollusc species. In all anadara tissues the intensity of LPO processes was lower than that in Mytilus galloprovincialis. The GP activity in hepatopancreas and gills of mussels was significantly higher than that of anadara. On the contrary, in the foot the GP activity and GSH content in anadara considerably exceeded those in mussel. The revealed differences might reflect the peculiarities in functioning of the glutathione complex and the ratio of its activity with LPO level in tissues of anadara and mussel, as well as be of interest for understanding mechanisms of mollusc adaptation to their habitat conditions.     

Zn Subcellular Distribution in Liver of Goldfish (Carassius Auratus) with Exposure to Zinc Oxide Nanoparticles and Mechanism of Hepatic Detoxification

Zinc Oxide Nanoparticles (ZnO NPs) have attracted increasing concerns because of their widespread use and toxic potential. In this study, Zn accumulations in different tissues (gills, liver, muscle, and gut) of goldfish (Carassius auratus) after exposure to ZnO NPs were studied in comparison with bulk ZnO and Zn²⁺. And the technique of subcellular partitioning was firstly used on the liver of goldfish to study the hepatic accumulation of ZnO NPs. The results showed that at sublethal Zn concentration (2 mg/L), bioaccumulation in goldfish was tissue-specific and dependent on the exposure materials. Compared with Zn²⁺, the particles of bulk ZnO and the ZnO NPs appeared to aggregate in the environmentally contacted tissues (gills and gut), rather than transport to the internal tissues (liver and muscle). The subcellular distributions of liver differed for the three exposure treatments. After ZnO NPs exposure, Zn percentage in metal-rich granule (MRG) increased significantly, and after Zn²⁺ exposure, it increased significantly in the organelles. Metallothionein-like proteins (MTLP) were the main target for Zn²⁺, while MRG played dominant role for ZnO NPs. The different results of subcellular distributions revealed that metal detoxification mechanisms of liver for ZnO NPs, bulk ZnO, and Zn²⁺ were different. Overall, subcellular partitioning provided an interesting start to better understanding of the toxicity of nano- and conventional materials.     

Induction of metallothionein-like proteins by mercury and distribution of mercury and selenium in the cells of hepatopancreas and gill tissues in mussel Mytilus galloprovincialis

The binding of mercury (Hg) to metallothioneins (MTs) and the relation between Hg and selenium in supernatants of hepatopancreas and gill tissues of the common mussel Mytilus galloprovincialis (Lamarck, 1819) was investigated. The mussels were exposed to different Hg concentrations in laboratory conditions: 2.5 μgHg/L, 4 d exposure (short term) and 60 μgHg/L, 33 d exposure (long term). In addition, the results were compared to those found for mussels from nature (polluted and unpolluted region). In control and short-term-exposed mussles, the level of Hg extraction (cytosol) from hepatopancreas and gill cells was very low with respect to the total Hg concentrations in the corresponding tissues, around 10% in control and around 20% after exposure. As expected, Hg exposure was followed by Se increase. For Se, the levels of extraction were higher, around 20% in control and up to 50% (heaptopacrease) of 70% (gills) after exposure. In order to study the distribution of Hg and Se in the cells of these organs, the total Hg and Secconcentrations were analyzed in the subcellular fractions obtained after differential centrifugation. Although after exposure the concentrations of both element increased in all subcellular fractions, their percentages in particular fractions were lower or higher. In this study, the convincing binding of Hg to metallothionein-like proteins was perceived after long-term laboratory exposure (gills, heapatopancreas) and in wild mussels collected near industrial port (hepatopancreas). In latter case, we also detected the traces of Se bound to the MT fractions after size-exclusion chromatography.     

The effects of zinc oxide nanoparticles on the metallome in freshwater mussels

The use of zinc oxide nanoparticles (nanoZnO) as sunscreens has raised concerns about their safety and release in the aquatic environment through swimming activities and within municipally treated wastewaters. This study's purpose was to examine the effects of nanoZnO on the elemental composition (metallome) in exposed freshwater mussels, Elliptio complanata. Mussels were exposed for 21 days to an environmentally realistic (low) concentration (2 μg/L) of nanoZnO and zinc chloride. The mussels were also exposed to a physically and chemically treated municipal effluent (ME), both alone and in the presence of both forms of Zn. The metallome profile was characterized by the following 15 elements in gills, digestive gland and gonad tissues: Ag, Al, As, Cd, Co, Cr, Cu, Fe, Mn, Mo, Ni, Pb, Se, V and Zn. The levels of metallothioneins (MT) and lipid peroxidation (LPO) in the digestive gland were also measured as biomarkers of toxic effects. The data revealed that exposure to nanoZnO increased the total levels of Zn, MT and LPO in the digestive gland. Discriminate function analysis revealed that the digestive gland responded the most to exposure to either nanoZnO or Zn^2 +. For nanoZnO, the observed changes in Al, As and Mo in the digestive gland offered the best discrimination from dissolved Zn^2 +. Co-exposure of nanoZnO with the ME changed the metallome profile closer to dissolved Zn^2 +, suggesting a common interaction site within the ME. This was observed in changes in Ni, Cu, Se and Zn in the digestive gland of exposed mussels. Canonical analysis of essential and non-essential elements revealed that exposure to nanoZnO increased the relationships between LPO and the sum of essential elements in the digestive gland. Conversely, exposure to dissolved Zn^2 + and the ME decreased the relationship between the sum of non-essential elements and LPO and MT. In conclusion, the use of a “metallomic” approach was used to discriminate changes following exposure to nanoZnO and dissolved Zn in freshwater mussels and provided insights into the interaction of forms of Zn in ME towards mussels.     

Cheating the Locals: Invasive Mussels Steal and Benefit from the Cooling Effect of Indigenous Mussels

The indigenous South African mussel Perna perna gapes during periods of aerial exposure to maintain aerobic respiration. This behaviour has no effect on the body temperatures of isolated individuals, but when surrounded by conspecifics, beneficial cooling effects of gaping emerge. It is uncertain, however, whether the presence of the invasive mussel Mytilus galloprovincialis limits the ability of P. perna for collective thermoregulation. We investigated whether varying densities of P. perna and M. galloprovincialis influences the thermal properties of both natural and artificial mussel beds during periods of emersion. Using infrared thermography, body temperatures of P. perna within mixed artificial beds were shown to increase faster and reach higher temperatures than individuals in conspecific beds, indicating that the presence of M. galloprovincialis limits the group cooling effects of gaping. In contrast, body temperatures of M. galloprovincialis within mixed artificial mussel beds increased slower and exhibited lower temperatures than for individuals in beds comprised entirely of M. galloprovincialis. Interestingly, differences in bed temperatures and heating rates were largely dependent on the size of mussels, with beds comprised of larger individuals experiencing less thermal stress irrespective of species composition. The small-scale patterns of thermal stress detected within manipulated beds were not observed within naturally occurring mixed mussel beds. We propose that small-scale differences in topography, size-structure, mussel bed size and the presence of organisms encrusting the mussel shells mask the effects of gaping behaviour within natural mussel beds. Nevertheless, the results from our manipulative experiment indicate that the invasive species M. galloprovincialis steals thermal properties as well as resources from the indigenous mussel P. perna. This may have significant implications for predicting how the co-existence of these two species may change as global temperatures continue to rise.     

Multiple forms of metallothionein from the digestive gland of naturally occurring and cadmium-exposed mussels, Mytilus galloprovincialis

Polymorphism of metallothioneins in the digestive gland of naturally occurring (control) and experimentally Cd-exposed mussels Mytilus galloprovincialis (200 μg Cd l^–1; 14 days) was studied by applying the conventional methods of Sephadex column liquid chromatography (G-75 and DEAE A-25), and by an electrochemical method (DPASV) for determination of Cd, Zn and Cu concentrations in chromatographic fractions. In both control and Cd-exposed mussels, two distinct molecular mass components of the metallothioneins, monomeric (MT-10) and dimeric (MT-20), were resolved by Sephadex G-75 gel filtration chromatography. In control mussels, the MT-10 component was predominantly expressed as containing markedly higher constitutive levels of Zn (100×) and Cu (10×) than of Cd. Each of these two molecular mass components was further resolved into seven metal-rich peaks by anion-exchange chromatography. In Cd-exposed mussels the larger proportion of Cd was bound to the MT-20 than to the MT-10 component, suggesting that the dimeric component may be considered as a primarily inducible metallothionein. The elution positions of metal-binding maxima of Cd-exposed and control mussels on the respective DEAE chromatographic profiles were comparable. A great similarity in elution positions of Cd maxima between the composite and single-specimen samples was also observed. Our study confirms a high multiplicity of MT forms in mussels from the Mytilus genus not only under the laboratory high-level metal exposure conditions, but also at a natural seawater metal exposure level. The ecotoxicological significance of dimeric and monomeric MT forms, as well as their possible application in the biomonitoring of seawater for trace metals, has been considered. Electronic Publication     

Metallothionein response to cadmium and zinc exposures compared in two freshwater bivalves, Dreissena polymorpha and Corbicula fluminea

Metallothionein (MT) response to cadmium (Cd) and zinc (Zn) bioaccumulation after single or combined direct exposure was compared in two freshwater bivalves, Dreissena polymorpha (zebra mussel) and Corbicula fluminea (Asiatic clam). Bivalves were exposed to 0.133 μM Cd and/or 15.3 μM Zn, with metal and MT concentrations analysed in the whole soft body after 1, 3, 10 and 24 days of exposure and compared with controls. Results showed significant increase in MT concentrations in both species exposed to Cd and Cd+Zn with a higher accumulation of the protein compared to the control in D. polymorpha for nevertheless similar Cd levels accumulated with time. Exposure to Zn alone led to a significant increase in MT concentrations only in C. fluminea, whereas there was a lack of MT gene induction in the zebra mussels which was confirmed by MT mRNA quantification in gills (RT-PCR). Mussel mortality after 10 days of exposure to Zn and Cd + Zn is discussed with regard to detoxification mechanisms, which include metallothioneins.     

Toxicity of lead and zinc to developing mussel and sea urchin embryos: Critical tissue residues and effects of dissolved organic matter and salinity

Lead (Pb) EC50 values in the very sensitive early development phases (48–72 h post-fertilization) of the mussels Mytilus galloprovincialis and Mytilus trossolus and sea urchin Strongylocentrotus purpuratus in 100% sea water were: M. trossolus — 45 (95% C.I. = 22–72) μg L^− 1; M. galloprovincialis — 63 (36–94) μg L^− 1; S. purpuratus — 74 (50–101) μg L^− 1. Salinity thresholds for normal development varied: M. trossolus > 21 ppt; M. galloprovincialis > 28 ppt; S. purpuratus ≥ 30 ppt. Addition of two spectroscopically distinct dissolved organic matters (DOM) from fresh water (Nordic Reservoir) and sea water (Inshore) moderately decreased the toxicity of Pb to both mussels, but not in a concentration-dependent fashion, with only an approximate doubling of EC50 over the range of 1.4–11.2 mg C L^− 1. Independent Pb binding capacity determinations for DOC explained the lack of a relationship between DOM concentration and toxicity. Salinity had no effect on Pb toxicity down to 21 ppt in M. trossolus, and low salinity (21 ppt) did not enhance the protective effect of DOC. Both DOMs increased the toxicity of Pb in developing sea urchin embryos, in contrast to mussels. Relative to Pb, the organisms were 6–9 fold less sensitive to Zn on a molar basis in 100% seawater with the following Zn EC50s: M. trossolus — 135 (103–170) μg L^− 1; M. galloprovincialis — 172 (126–227) μg L^− 1, S. purpuratus — 151 (129–177) μg L^− 1. Nordic Reservoir and Inshore DOM (2–12 mg C L^− 1) had no significant effect on Zn toxicity to mussels, in accord with voltammetry data showing an absence of any strong ligand binding for Zn by DOMs. As with Pb, DOMs increased Zn toxicity to urchin larvae. Critical Tissue Residues (CTR) based on whole body concentrations of Pb and Zn were determined for M. galloprovincialis at 48 h and S. purpuratus at 72 h. The median lethal CTR values (LA50s), useful parameters for development of saltwater Biotic Ligand Models (BLMs), were approximately 4-fold higher on a molar basis for Zn than for Pb. The latter were not altered by DOM exposure, despite increased EC50 values, in accord with the tenets of the BLM.     

Biochemical characterization of the DNA polymerase activity present in isolated nuclei from mussel tissues: a possible system for the evaluation of the rate of DNA repair

1. The nuclear DNA polymerase activity in mussel digestive glands was characterized regarding Mg++ requirement (2 mM), ATP concentration (4 mM), pH (8.4), and ionic strength (50 mM). 2. Most of the enzymatic activity is aphidicolin insensitive, probably due to DNA polymerase beta-like activity. 3. The exposure of mussels to a genotoxic organic compound such as dimethylsulfate (DMS) resulted in increases of about 250% and 100% in the DNA polymerase activity in nuclei isolated from the gills and digestive glands, respectively. 4. These data indicate that the isolated nuclei from mussel tissues may be utilized for the evaluation of the rate of DNA repair synthesis that reflects the DNA damage induced in vivo by exposure of the animals to genotoxic compounds.     

Heavy metal effects on lipid peroxidation in the tissues of mytilus gallopro vincialis lam.

1. The effects of heavy metals on lipid peroxidation in the gills and digestive gland of mussels exposed for six days to Cu²⁺, Cd²⁺ or Zn²⁺ (40 μg/l/animal) were investigated.2. In the tissues of Cu-exposed mussels a significant increase of the level of malondialdehyde (MDA), which is indicative of the peroxidative process, and a decrease of the concentration of glutathione were observed.3. Moreover, in the digestive gland of mussels, copper exposure results in an increase of other carbonyl compounds and in the lysosomal accumulation of lipofuscin granules.4. The exposure of mussels to Zn or to Cd did not elicit any of the above effects.5. The results are discussed in relation to the possible role that Cu-induced lysosomal lipofuscin accumulation may play in heavy metal detoxification.     

Variation in scope for growth: a test of food limitation among intertidal mussels

Wellington Harbour supports large populations of the mussels Aulacomya maoriana, Mytilus galloprovincialis and Perna canaliculus that are almost entirely absent from nearby coastal locations in Cook Strait. We calculated scope for growth (SFG) using ambient Cook Strait water over a broad temporal scale and a broad range of seston conditions to determine if negative SFG explains this phenomenon. Although all three mussel species had positive mean SFG values, variation in SFG was high and negative values often occurred: A. maoriana 19.1 J g⁻¹ h⁻¹, 43% of mussels showed negative SFG; M. galloprovincialis 1.26, 52% negative SFG; P. canaliculus 45.6, 27% negative SFG. Negative SFG was most often due to negative absorption efficiency caused by metabolic faecal loss that is characteristic of mussels feeding in environments with low seston quality. From our ecophysiology data we constructed a model to estimate SFG based on physiological responses to the narrow range of seston conditions typical of Cook Strait (Model One), and a model to estimate SFG based on physiological responses of mussels to the broad range of seston conditions typical of Wellington Harbour and Cook Strait (Model Two). We used seston data collected over an 18-month period from sites in Wellington Harbour and Cook Strait to derive 159 estimates of species-specific mussel SFG from both models. Both models produced higher estimates of SFG for mussels in the Harbour compared with those at Cook Strait sites. This was consistent with elevated particulate concentrations in the Harbour than at Cook Strait sites, and in agreement with previous studies. For Cook Strait mussels, both models produced negative estimates of net energy balance for long periods of time (several months), whereas for Harbour mussels negative SFG estimates were generally short in duration. We conclude that our short-term laboratory-based determinations of SFG and our long-term bioenergetics modelling estimates do not conclusively support the hypothesis of food limitation for three coexisting taxa of mussels in the intertidal region of Cook Strait, New Zealand. Handling editor: P. Viaroli     

Investigation of the effects of current velocity on mussel feeding and mussel bed stability using an annular flume

An annular flume was used to measure the effect of increasing current velocity on mussel (Mytilus edulis) feeding rate and the stability of mussel beds sampled from the mouth of the Exe estuary (SW England). It was found that, in contrast to earlier flume studies, the feeding rates of mussels from open coast sites were unaffected by current velocities up to 0.8 m s^–1. Algal cell depletion in the water column above mussels was a function of current velocity, increasing with declining currents below 0.05 m s^–1. The erodability/stability of the mussel bed, measured in terms of critical erosion velocity, sediment mass eroded and mean erosion rate, was found to be a function of the nature of the substrate and the density of the mussels. Erosion of mussel beds on sandy substrate showed a non-linear relationship with mussel bed density. In comparison with the sand (0% mussel cover), sediment resuspension was about five and four times higher for 25% and 50% cover, respectively. This was due to the increased turbulence and scouring around the clumps of mussels in low-density parts of the bed, and this resulted in some mussels detaching from the bed. At ~100% mussel cover, the sandy bed was more protected by the dense surface layer of mussels, and none became detached during erosion due to the high number of byssal attachments between individuals. The sediment resuspension from the 100% mussel cover was about three times lower than the 0% cover. Erosion of the bed with 50% cover resulted in burial of a large proportion of the mussels, with a 6 cm increase in sediment level. However, the mussels returned to the surface and recovered in 1–2 days, due to a combination of migration upwards and substrate settlement. Channels on the edge of the main Exmouth mussel bed were characterised by a more stable substrate comprising pebbles and sand with varying mussel densities. At these sites, where mussels experience high current velocities on spring tides (up to 0.9 m s^–1), there was no difference between the erodability of pebble/sand substrate with 0% and 100% mussel cover. The sediment erosion was also lower than the 100% mussel cover on the sandy substrate, particularly at currents >0.4 m s^–1. Sampling of different parts of the mussel bed at Exmouth showed mussels at low densities were made up of smaller clumps with a lower mass ratio of mussels to attached substrate (pebbles/sand), thus providing a greater degree of anchorage. Electronic Publication     

Comparison of phototrophic shell-degrading endoliths in invasive and native populations of the intertidal mussel Mytilus galloprovincialis

The intertidal mussel Mytilus galloprovincialis is a successful invader worldwide. Since its accidental introduction onto the South African west coast in the late 1970s, it has become the most successful marine invasive species in South Africa. One possible explanation for this phenomenon is that M. galloprovincialis suffers less from phototrophic shell-degrading endoliths in its invasive than in its native range. We assessed photoautotrophic endolithic pressure on M. galloprovincialis in native (Portugal) and invasive (South Africa) ranges. Invasive populations were more heavily infested than native populations. In Portugal, only the biggest/oldest mussels displayed endolithic erosion of the shell and the incidence of infestation was greater at higher shore levels where more prolonged exposure to light enhances endolith photosynthesis. In South Africa, even the smallest size classes of mussels were heavily infested throughout the shore. In Portugal, endolithic-induced mortality was observed at only one location, while in South Africa it occurred at all locations and at significantly higher rates than in Portugal. Important sub-lethal effects were detected in infested native mussels, confirming previous studies of invasive populations and suggesting an energy trade-off between shell repair and other physiological constraints. We observed a positive relationship between infestation rates and barnacle colonization on mussel shells, suggesting possible facilitation of barnacle settlement/survival by shell-boring pathogens. Identification of endoliths revealed common species between regions. However, two species were unique in the invasive range while another was unique in the native region. Different levels of endolithic infestation in the invasive and the native range were not explained by the effect of major environmental determinants (Photosynthetically Available Radiation and wave height). The results reject our initial hypothesis, indicating that invasion success of M. galloprovincialis is not simply explained by escape from its natural enemies but results from complex interactions between characteristics of the invaded community and properties of the invader.     

An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.