Siphon size and burying depth in deposit- and suspension-feeding benthic bivalves

This paper analyses the significance of siphon investment in the life strategy of benthic bivalves. It describes the relationships between siphon weight, burying depth and shell size in Mya arenaria, Cerastoderma edule. Scrobicularia plana and Macoma balthica. All data were collected on an intertidal flat in the Dutch Wadden Sea during seven successive winter and summer periods. The four species have in common that (1) the increase of depth in relation to size can be described with an S-curve; (2) there is a linear relationship between log siphon weight and log shell size; (3) siphon investment is maximal for the size classes with the greatest increase in their depth; (4) siphon weight, in proportion to total body weight, decreases gradually for the larger size classes whose depth does not increase; (5) burying depth increases with siphon weight if individuals within a same size class are compared, but burying depth levels off above a certain siphon weight. Macoma balthica and Scrobicularia plana live twice as deep in winter as in summer, although siphon weight for both seasons is about the same. In summer both species use a part of the siphon to graze the surface around the burrow, whereas deposit feeding does not occur in winter. This might explain the seasonal variation in burying depth. On the other hand Cerastoderma edule and Mya arenaria, which are both suspension feeders, show hardly any increase of depth in winter as compared to summer. For benthic bivalves the risk of being taken by a predator decreases with depth. The burying depth levels off where individuals reach the depth refuge (though in winter Scrobicularia plana live at greater depth). The conclusion is that siphon size is one of the main factors determining the burying depth of benthic bivalves and thus plays a critical role in their survival.     

Effect of periphyton grazing by Hydrobia ulvae on the growth of Zostera noltii on a tidal flat in the Dutch Wadden Sea

The decrease of the intertidal seagrass Zostera noltii in the Dutch Wadden Sea may have been the result of enhanced periphyton load due to eutrophication. Decrease of this seagrass species coincided with an increase in the mudsnail Hydrobia ulvae. Feeding of this mudsnail on periphyton may have partly counteracted an increase of periphyton biomass. Exclosure experiments on seagrass stands in the Dutch Wadden Sea in 1987 showed that density of periphyton on leaves of Z. noltii decreased significantly with increasing density of grazers. An increased density of mudsnails significantly enhanced the density and biomass of seagrass, in particular of the below ground parts. Since this seagrass species survives winter in temperate climate zones mainly by means of rhizomes, grazing may also influence the seagrass dynamics in the long term. Results of the experiment were in agreement with field observations on coinciding low densities of mudsnails and high densities of fouling of seagrass stands on the tidal flats of western Wadden Sea in the late 1970s.     

Human trampling as short-term disturbance on intertidal mudflats: effects on macrofauna biodiversity and population dynamics of bivalves

The effect of physical disturbance in the form of trampling on the benthic environment of an intertidal mudflat was investigated. Intense trampling was created as unintended side-effect by benthic ecologists during field experiments in spring and summer 2005, when a mid-shore area of 25 × 25 m was visited twice per month by on average five researchers for a period of 8 months. At the putatively-impacted location (I) (25 × 25 m) and two nearby control locations (Cs) (25 × 25 m each), three sites (4 × 4 m) were randomly selected and at each site, three plots (50 × 50 cm) were sampled after 18 and 40 days from the end of the disturbance. Multivariate and univariate asymmetrical analyses tested for changes in the macrofaunal assemblage, biomass of microphytobenthos and various sediment properties (grain-size, water content, NH₄ and NO₃ concentrations in the pore water) between the two control locations (Cs) and the putatively-impacted location (I). There were no detectable changes in the sediment properties and microphytobenthos biomass, but variability at small scale was observed. Microphytobenthos and NH₄ were correlated at I to the number of footprints, as estimated by the percentage cover of physical depressions. This indicated that trampling could have an impact at small scales, but more investigation is needed. Trampling, instead, clearly modified the abundance and population dynamics of the clam Macoma balthica (L.) and the cockle Cerastoderma edule (L.). There was a negative impact on adults of both species, probably because footsteps directly killed or buried the animals, provoking asphyxia. Conversely, trampling indirectly enhanced recruitment rate of M. balthica, while small-sized C. edule did not react to the trampling. It was likely that small animals could recover more quickly because trampling occurred during the growing season and there was a continuous supply of larvae and juveniles. In addition, trampling might have weakened negative adult-juvenile interactions between adult cockles and juvenile M. balthica, thus facilitating the recruitment. Our findings indicated that human trampling is a relevant source of disturbance for the conservation and management of mudflats. During the growing season recovery can be fast, but in the long-term it might lead towards the dominance of M. balthica to the cost of C. edule, thereby affecting ecosystem functioning.     

Minimal predation upon meiofauna by endobenthic macrofauna in the Exe Estuary,south west England

Field manipulation experiments were performed in the Exe Estuary, south west England, in October 1988, to investigate the importance of the meiofaunamacroinfauna trophic link in benthic trophodynamics. Four hypothetically meiofauna-predacious endobenthic macrofauna species were selected for manipulation using the criteria of high abundance and different modes of feeding: Cerastoderma edule (filter-feeder), Nereis diversicolor (omnivorous scavenger), Ophelia bicornis (sand-ingester), Scrobicularia plana (deposit-feeder). Enclosures constructed from plastic tubing, 63 m nylon monofilament mesh and galvanized steel were deployed, containing adult members of these taxa at densities raised to approximately four times that of the surrounding sediment. The experiments ran for 12 tidal cycles. Differences in phyletic meiofaunal abundance between treatment and control enclosures at the termination of the experiment were assessed using both uni- and multivariate dataanalysis techniques. Only two univariate significant differences (p<0.05) existed for the N. diversicolor treatment and two for the S. plana treatment. Annelida, Turbellaria and copepod nauplii were the only meiofauna taxa affected. No univariate significant differences were recorded for either the C. edule or O. bicornis treatments. Multidimensional scaling ordination of the data revealed no consistent changes in community composition between treatments and controls. It is concluded that the experiments provide evidence of minimal predation by macroinfauna upon meiofauna.     

An electron-microscope study of periostracum formation in some marine bivalves. I. The origin of the periostracum

Electron microscopy has revealed the presence of specialised basal cells at the base of the periostracal groove in the bivalves Mytilus edulis (L), Nucula sulcata Bronn., Cardium edule (L) and Macoma balthica (L). A common basal cell type is observed which gives rise to a pellicle in all cases except N. sulcata. The pellicle is the first part of the periostracum to be elaborated, and it is suggestd that it may be an indication of specialisation in bivalves. In N. sulcata and C. edule, an additional cell type is present. In N. sulcata, this second basal cell type appears to be directly involved in periostracum formation, whereas in C. edule an indirect role is proposed.     

Patterns of organic osmolytes in two marine bivalves, Macoma balthica, and Mytilus spp., along their European distribution

Patterns of nine intracellular free amino acids (FAA), which are utilized as organic osmolytes for salinity-induced cell volume regulation in marine osmoconformers, were compared in five Macoma balthica populations and seven Mytilus spp. populations along their European distribution. Three types of FAA patterns were classified within both taxa: a northern Baltic type, a southern Baltic type and an Atlantic/Mediterranean type which mainly differ regarding the share of alanine and taurine. Differences are discussed in relation to habitat salinity and population genetics. Along a salinity gradient, the total size of the intracellular FAA pool did not differ between sympatric M. balthica and Mytilus spp., and was significantly correlated with habitat osmolality in a range from 70 to 600 mmol kg⁻¹ H₂O (oligohaline to mesohaline) in both bivalves. In M. balthica, this correlation was mainly based on significant correlations of alanine (15–100 mmol kg⁻¹ DW), glycine (30–100 mmol kg⁻¹ DW) and taurine (0–70 mmol kg⁻¹ DW) with habitat osmolality. In Mytilus spp., only glycine (25–100 mmol kg⁻¹ DW) and taurine (4–180 mmol kg⁻¹ DW) were significantly correlated with habitat osmolality. The concentration of alanine was three times lower in Mytilus spp. than in M. balthica and did not correlate with habitat osmolality. Within a habitat osmolality range from 600 to 1,100 mmol kg⁻¹ H₂O (mesohaline to marine) the concentration of FAA remained constant in both taxa. It is suggested that under marine conditions additional organic osmolytes must become more important for cell volume regulation in Macoma and Mytilus.     

Accumulation of polychlorinated biphenyls in the cockle Cerastoderma edule and the tellin Macoma balthica

Two species of marine bivalve, Cerastoderma edule (Linnaeus) and Macoma balthica (Linnaeus), were exposed to particles contaminated with three commercial polychlorinated biphenyl (PCB) mixtures, Aroclors^® 1242, 1254 and 1260. The accumulation of PCB in bivalve tissue was monitored for periods of up to 40 days. In addition to measuring total PCB concentrations, which reached 60 ppm of Aroclor 1242 in M. balthica, the fate of individual PCB homologues of different chlorine content, ranging from 2 to 8 chlorine atoms per biphenyl molecule, was also determined. Selective accumulation of PCBs with 5 chlorine atoms per biphenyl molecule occurred, whilst isomers of very low and very high molecular weights were accumulated at much slower rates.     

An electron-microscope study of periostracum formation in some marine bivalves. II. The cells lining the periostracal groove

The histology and ultrastructure of the epithelial cells of the outer and middle mantle folds of the bivalves Mytilus edulis (L), Cardium edule (L), Macoma balthica (L) and Nucula sulcata Bronn are described. The cells lining the inner face of the outer fold exhibit a prominent granular endoplasmic reticulum, and Golgi complexes which are concerned with the elaboration of granules and vesicles eventually incorporated into the periostracum. A gradual reduction in the protein synthetic apparatus occurs towards the tip of the fold. Within the cells, it is proposed that the ovoid inclusion bodies are lysosomes and that they control the rate of secretion. The cells of the middle fold are cuboidal in appearance. Those of M. edulis and N. sulcata exhibit prominent granules, whereas those of C. edule and M. balthica possess vesicles. The cells of M. edulis differ from the others in possessing stout bundles of filaments, which occupy large areas of the cell and constitute a cell web. The cells of the epithelium in all cases do not appear to be implicated in periostracum formation.     

Natural variability in distribution of an intertidal population of Macoma balthica subject to potential oil pollution at Port Valdez,Alaska

Natural variability in the abundance of an intertidal population of the lamellibranch Macoma balthica (Linnaeus, 1758) was measured during 1971 and 1972 in a study area near the proposed oil storage and tankship loading facility at the southern terminus of the Trans-Alaska pipeline in Port Valdez, Alaska. M. balthica were divided for analysis into a large and a small size category. Small temporal changes in population densities throughout the entire study area were detected for both size categories over several of the 7 sampling times of the 2-year period. Large and persistent differences in density were found among elevation contour intervals for either size category; however, variations in the density profiles on elevation occurred among sampling times. Large M. balthica became more equitably distributed and the small category less equitably distributed among elevation contours over the 2-year period. Densities of both size categories were more stable at the higher elevations of the study site. Large M. balthica were more homogeneously distributed along a given elevation contour interval than the small category. Mobility and time available to redistribute at a horizontal location would explain the more homogeneous distribution of large M. balthica if competition for food resources exists.     

Single-step nested multiplex PCR to differentiate between various bivalve larvae

A nested multiplex polymerase chain reaction (PCR) assay has been developed that allows the discrimination between six bivalve larvae common to Danish coastal waters (Cerastoderma edule, Macoma balthica, Mytilus edulis, Spisula subtruncata, Ensis americanus and members of the order Myoida). This assay involves the simultaneous use of a pair of general universally targeted 18S rRNA gene primers, five specific 18S rRNA gene targeted oligonucleotide primers internal (nested) to the universal primer pair and one species-specific primer that is not nested (Mya). The specificity of each primer was evaluated in silico, empirically, and verified further by sequencing of amplification products from single larvae collected from plankton samples. Identification of individually isolated bivalve larvae from plankton samples was based on the size of the PCR product produced by the specific primers after visualisation by agarose gel electrophoresis. Preliminary studies indicated that this method was suitable for use with freshly collected and preserved larvae, and is therefore suitable for field application.Communicated by M. Kühl, Helsingør     

Upper temperature tolerances of Tellina tenuis and T. fabula

The upper lethal tolerances of Tellina tenuis da Costa and T. fabula Gmelin were studied under a variety of temperature regimes in which both short-term and long-term mortality were noted; these included steady temperatures, acclimation at a steady temperature then exposure to a steady tempeature, and acclimation at gradually increasing temperatures. T. tenuis alone was also tested for variation in mortality rate according to the date of collection or to the size (i.e., age) of the mollusc. The results suggested that T. tenuis was consistently more tolerant than T. fabula, and that the difference in tolerance was around 5 C°. Both species readily acclimated to higher temperatures after steady temperature acclimation, but not under a regime of gradually increasing temperature. There was no significant, variation in the mortality rate of T. tenuis with season or age. It is suggested that, since the difference in temperature tolerance is not reflected in their respective geographical distributions, there may be some other stage in their life cycle, e.g. the larvae, which is equally susceptible to temperature extremes. The difference in tolerance is, however, reflected in their respective littoral and sublittoral distributions.     

Spatial variability of length-specific production in shell,somatic tissue and sexual products of Macoma balthica in the Lower St. Lawrence Estuary

A field study on the spatial variability of production and some demographic parameters was conducted in 1988 in ten populations of Macoma balthica located on the north and south shores along the entire length (230 km) of the Lower St. Lawrence Estuary (LSLE, Canada) at the same intertidal level. Standard-length estimates (10 mm) of shell and somatic tissue production for the period of May to November were highly variable between stations and greater on the north shore than on the south shore. Standard-length estimates of the gamete production for the period of July to November were also highly variable between stations but there was no variation between shores. The inter-population variability of the standard-length estimates of production in shell, somatic tissue and sexual products was as large as the intrapopulation variability between both the upper and lower tidal levels measured in previous studies. There were no significant linear relationships between standard-length estimates of production and biotic (density) or abiotic (temperature, chlorophyll-a in top sediment, mean phi, water salinity) factors, but we observed some significant quadratic relationships between standard-length estimates of production and mean sediment-surface temperature during the growing season. The standard-length estimates of production were lower at the coldest and warmest stations than at the more temperature stations. There was also a significant negative linear relationship between mean sediment-surface temperature during the growing season and the grain size structure of sediment, indicating that the sediment texture, indirectly, largely influenced the inter-station and the inter-shore variability of production in shell, somatic tissue and sexual products of M. balthica in the LSLE.     

Settlement of <Emphasis Type="Italic">Macoma balthica</Emphasis> larvae in response to benthic diatom films

The role of multi-species benthic diatom films (BDF) in the settlement of late pediveliger larvae of the bivalve Macoma balthica was investigated in still-water bioassays and multiple choice flume experiments. Axenic diatom cultures that were isolated from a tidal mudflat inhabited by M. balthica were selected to develop BDF sediment treatments characterized by a different community structure, biomass, and amount of extracellular polymeric substances (EPS). Control sediments had no added diatoms. Although all larvae settled and initiated burrowing within the first minute after their addition in still water, regardless of treatment, only 48–52% had completely penetrated the high diatom biomass treatments after 5 min, while on average 80 and 69% of the larvae had settled and burrowed into the control sediments and BDF with a low diatom biomass (<3.5 μg Chl a g⁻¹ dry sediment), respectively. The percentage of larvae settling and burrowing into the sediment was negatively correlated with the concentration of Chl a and EPS of the BDF. This suggests higher physical resistance to bivalve penetration by the BDF with higher diatom biomass and more associated sugar and protein compounds. The larval settlement rate in annular flume experiments at flow velocities of 5 and 15 cm s⁻¹ was distinctly lower compared to the still-water assays. Only 4.6–5.8% of the larvae were recovered from BDF and control sediments after 3 h. Nonetheless, a clear settlement preference was observed for BDF in the flume experiments; i.e., larvae settled significantly more in BDF compared to control sediments irrespective of flow speed. Comparison with the settlement of polystyrene mimics and freeze-killed larvae led to the conclusion that active selection, active secondary dispersal and, at low flow velocities (5 cm s⁻¹), passive adhesion to the sediment are important mechanisms determining the settlement of M. balthica larvae in estuarine biofilms.     

Effects of Lunatia heros predation on the population dynamics of Mya arenaria and Macoma balthica in Maine,USA

The interaction between the naticid snail predator Lunatia heros and 2 iteroparous, infaunal, intertidal bivalves was investigated in Lubec, Maine, USA. The Mya arenaria population consists primarily of young, small individuals. M. arenaria survivorship is low when young (3.5% yr^-1 for the first 5 yr), then increases. M. arenaria can attain a length of 60 mm, but it is susceptible to L. heros attack only until it is 30 mm long. It delays reproduction until it is 20 mm long (3.8 yr) and diverts its resources instead into rapid early growth (4.9 mm yr^-1 for the first 5 yr). The Macoma balthica population has a larger proportion of older individuals than does that of M. arenaria. Survivorship is higher for M. balthica than for M. arenaria (76.3% yr^-1 for the first 5 yr). Unlike M. arenaria, M. balthica attains a final length of only 25 mm and all sizes are susceptible to L. heros attack. M. balthica grows slowly (2.7 mm yr^-1 for the first 5 yr) and diverts its resources into earlier reproduction at a length of 10 mm (2.9 yr). These contrasting life-history patterns and the possible relationship between bivalve resource allocation and refuges from predation are discussed.     

Upper temperature tolerances of some European molluscs

The upper temperature tolerances of three European species of Cardium [C. (Cerastoderma) glaucum Bruguière, C. tuberculatum L., C. (Cerastoderma) edule L.] are compared by means of median lethal temperature (LT₅₀) and median burial temperature (BT₅₀) determinations for periods of exposure up to 96 h. The influence of previous acclimation temperatures on these determinations is also considered. C. glaucum from shallow water (0.5 to 1 m), lagoonal, habitats in the Mediterranean Sea shows a greater thermal tolerance than C. tuberculatum from deeper water (4 to 5 m) in the Mediterranean. The thermal tolerance of C. edule from the intertidal zone, but at higher latitudes, is intermediate. Young C. glaucum show a greater resistance to short exposures to high temperatures than adults, but for longer exposures their tolerance is the same. All 3 species exhibit a significant effect of previous acclimation temperature on the burrowing response, and C. glaucum and C. tuberculatum a significant but lesser effect on LT₅₀. LT₅₀ determinations with C. edule showed secondary mortality effects which may have obscured any effect of acclimation temperature.     

Sublethal effects of chronic oil exposure on the intertidal clam Macoma balthica

When exposed to Prudhoe Bay crude oil in flowing seawater for 180 days, the small intertidal clam Macoma balthica showed behavioral, physical, physiological and biochemical changes. At a high concentration of oil in seawater (3.0 mg l^-1) burrowing rate decreased, respiration rate increased, growth was inhibited, and very high mortalities resulted. The lowest concentration of oil in seawater (0.03 mg l^-1) inhibited growth and caused reabsorption of gametes. One group of adverse oil effects which was related to sluggishness and disorientation of the clams appeared after a week of exposure to oil; another group related to a negative energy balance was not observed until 60 days. We conclude that chronic exposure of M. balthica to oil-in-seawater concentrations even as low as 0.03 mg l^-1 will, in time, lead to population decreases.Please address requests for reprints to Dr. D. G. Shaw at the Institute of Marine Science     

Habitat related growth and reproductive investment in estuarine waters,illustrated for the tellinid bivalve <Emphasis Type="Italic">Macoma balthica</Emphasis> (L.) in the western Dutch Wadden Sea

In estuarine areas, bivalve species can be found in a variety of environments, where they experience large differences in environmental conditions. In the present paper, the importance of different habitats (intertidal, subtidal and adjacent coastal waters) for the persistence of the population was evaluated for the bivalve Macoma balthica (L.) in the western Dutch Wadden Sea estuary. Intra-specific variation in growth and reproductive output were followed during the year and related to local abiotic conditions. Significant differences in growth and reproductive investment were found between locations. Young individuals were mostly found in the intertidal area, where growth in terms of somatic mass was good. These areas were not favourable for adult individuals, since growth in shell length was low and many individuals did not reproduce. In the subtidal, where the highest densities were found, somatic and gonadal mass indices were low. Coastal areas had the lowest densities and showed high growth in terms of shell length and body mass. The habitat with the highest reproductive effort per individual was not the most important habitat in terms of reproductive output due to differences in density and in size of the habitat type. For M. balthica, the subtidal habitat contributed the most to the reproductive output of the western Dutch Wadden Sea population although the highest reproductive output per individual was in the coastal area.     

Active pelagic migrations of the bivalve Macoma balthica are dangerous

The bivalve Macoma balthica migrates twice during the benthic part of its life cycle. During the spring migration (May-June), the newly settled spat (0-group) migrates to the nurseries in the high intertidal. Seven to nine months later, the bivalves migrate back to the low tidal flats and the subtidal (winter migration, 1-group). Both 0- and 1-group M. balthica use byssus threads for active pelagic migrations. As many M. balthica disappear during these migrations, we examined experimentally the importance of predation on 0- and 1-group M. balthica. Laboratory experiments using a circular aquarium determined predation rates on buried (no current) and drifting (current) 0- and 1-group M. balthica by several fish species (plaice, flounder, goby and whiting) and the shore crab. Under illuminated conditions, more M. balthica were consumed when migrating than when buried, whereas there was no difference between experiments in conditions of darkness. For the 0-group, predation rates on migrating and buried M. balthica in the dark were lower than in the light. The stomachs of pelagic fish in the Wadden Sea and Oosterschelde estuary did not contain M. balthica during winter migration. In the Wadden Sea, 1-group M. balthica primarily migrated at night. In conclusion, enhanced predation on drifting, as compared to buried, M. balthica may be the mechanism that explains enhanced mortality during migration in light, and may explain why M. balthica mainly migrates at night in the field. As we found no M. balthica in stomachs of pelagic fish, we do not know whether predation on byssus drifting M. balthica exists in the field. There are, however, some indications for fish predation on infaunal polychaetes during pelagic migrations.     

Male mate choice and male–male competition in the hermit crab Pagurus nigrofascia: importance of female quality

Male mate choice has recently been reported in some animals with male–male competition. In the laboratory, we examined whether males choose their mates based on female quality that was indicated by body size and/or days to prenuptial molt, and the effects of female quality on male–male competition in the hermit crab Pagurus nigrofascia. We collected samples from April to May 2009 at an intertidal shore in Hokkaido, Japan (41°N, 140°E). When a male simultaneously encountered two receptive females in the mate choice experiment, males chose females which require less time to molt. When a male guarding a female with less time to molt was challenged by an intruder, the guarding male defended the female for a longer period and was more likely to win the contest. These results indicate that male P. nigrofascia use time to molt to discriminate between females.     

Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail—from small to large scale

Shorebird abundance and spatial distribution of larval trematodes in the New Zealand mudsnail, Zeacumantus subcarinatus, were investigated in soft-sediment intertidal bays within Otago Harbour, South Island, New Zealand. In a small-scale study, recruitment of trematodes to caged sentinel snails and the prevalence of infection in free-living snails were examined across a grid of fifteen 50×25 m plots arranged in a representative area of an intertidal bay, in relation to within-plot shorebird abundance (definitive hosts) and tidal height. In a large-scale study, natural spatial variation of larval trematodes in Z. subcarinatus was examined across 12 bays in relation to local abundance of shorebirds. Our results revealed that trematode prevalence in snails was positively correlated with bird abundance across bays (R ²=0.503, P=0.006). In contrast, despite a difference in bird abundance between tidal heights, there was no evidence that trematode prevalence reflected the spatial distribution of birds in the small-scale study, suggesting that factors related to differences in submersion time may override the differential input of trematode eggs from birds.