Tellinid Bivalve Macoma Balthica Research Articles

Annual and spatial variability in gains of body weight in Macoma balthica (L.): Relationships with food supply and water temperature

The present paper reports on the results of a long-term field study on the simultaneous influence of 2 environmental factors (temperature and food supply) on annual growth rates in the tellinid bivalve Macoma balthica. For >30y (1978–2009) we monitored twice-annually the weight changes of soft parts of individuals of known age at several permanent sampling stations located at Balgzand, an extensive (50km2) tidal flat area in the western Dutch Wadden Sea. Monthly data were available on mean water temperature and chlorophyll a (chl a) concentration from a nearby site in the main tidal inlet. Mean individual ash-free dry weights at ages of nearly 1 and of nearly 1.5y were assessed in February/March and in August, respectively. Such weights show a consistent annual pattern: they increase between late winter and early summer to decline for the remainder of the year. Annual multi-station means of the spring/summer individual weight gains were higher as chl a concentrations in the water had been higher and water temperatures had been lower for the growing season. These correlations proved to be stronger at sampling sites that were situated low in the intertidal zone close to the main tidal stream than at those high in the intertidal near the coast (where M. balthica obtain their food primarily by deposit feeding on benthic material). At the low off-shore sites, suspended algae are available for longer daily periods and their concentrations in flood water may be less depleted by grazers. The negative correlation between weight gain and water temperature may have been primarily based on the shortening of the M. balthica growing seasons in warm summers. We conclude that the present simultaneous trends of global warming and declining stocks of pelagic algae may affect M. balthica in the Wadden Sea in a similar, negative, way.

Effects of fine-scale environmental heterogeneity on local genetic structure in Macoma balthica from the Gulf of Gdañsk (southern Baltic Sea)

It is increasingly recognized that populations of marine organisms with potential for large-scale dispersal may exhibit fine-scale genetic structure. The Gulf of Gdansk (Poland) is an interesting setting to study fine-grained population structure in marine organisms as it is characterized by chronic anthropogenic pollution and strong salinity gradients. We investigated, at two nested spatial scales (35 and 7 km), genetic structure among populations of the infaunal tellinid bivalve Macoma balthica. The COI mitochondrial marker revealed a likely mix of evolutionary lineages in the Gulf, with no detectable spatial structure. Seven microsatellite markers detected weak population structure, separating deep and shallow populations within short distances (7 km) and assignment tests suggested asymmetric gene flow among these populations, with no shallow recruits being detected in deep waters. Given the specific environmental conditions encountered at deeper depths in the Gulf (increased salinity, lower temperatures, oxygen depletion, hydrogen sulfide pollution), we suggest that deeper populations may be subjected to local adaptation.

Some like it cold: populations of the tellinid bivalve Macoma balthica (L.) suffer in various ways from a warming climate

Because of its relatively low tolerance to elevated temperatures, Macoma balthica (L.) may be one of the first important marine species in temperate coastal areas to suffer from a warming climate. For the last few decades, the abundance of the species in the Dutch Wadden Sea has been se- riously declining. At lower latitudes, the southern edge of its range recently shifted several 100s of km to the north. To understand changes in abundance related to high temperatures, we studied short-term population responses to warmer than average seasons using data from a long-term (>35 yr) sampling program in the western Wadden Sea. The observed relationships included reduction of reproductive output and recruitment in years starting with mild winter-spring periods, reduction of adult survival in years with warm summers, reduction of annual migration in ~8 mo olds to more favourable areas in mild winters, reduction of growth rates in warmer than average growing seasons, and enhancement of seasonal weight loss in milder than average winters. We conclude that elevated temperatures nega- tively affect population dynamics of M. balthica in a number of ways, i.e. via recruitment or mortality as well as growth. These negative influences were observed already far below the upper lethal tem- perature of the species and in populations living ~1000 km poleward of the warm edge of the species' range. The outcome of M. balthica's energy balance appears to be decisive for their continued exis- tence by effects not only on individual weights but also on mortality as well as reproduction.

Habitat related growth and reproductive investment in estuarine waters, illustrated for the tellinid bivalve Macoma balthica (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.

Experimental effects of immersion time and water temperature on body condition, burying depth and timing of spawning of the tellinid bivalve Macoma balthica

The burying depth of many bivalve molluscs on intertidal mudflats varies throughout the year and differs between places. Many factors are known to influence burying depth on a seasonal or spatial scale, with temperature and tidal regime probably being very important. Burying depth, body condition and gonadal development of Macoma balthica were followed throughout winter and spring in an experiment in which water temperature and immersion time were manipulated. Unexpectedly, relative water temperature, in contrast to the prediction, did not generally affect body condition or burying depth. This was probably a consequence of the exceptionally overall low water temperatures during the experimental winter. Differences in temperature did, however, result in different timing of spawning: M. balthica spawned earlier at higher spring temperatures. Longer immersion times led to higher body condition only late in spring, but led to deeper burying throughout almost the whole period. There was no effect of immersion time on the timing of spawning. We conclude that a longer immersion time leads to deeper burying, independent of body condition. We also conclude that burying behaviour of M. balthica is not determined by the moment of spawning.

Large spatial variability in lifetime egg production in an intertidal Baltic tellin (Macoma balthica) population

The extent to which it pays settling larvae of marine benthic organisms to actively select the habitat where they will spend the rest of their life can only be fully appreciated if the fitness consequences of such habitat selection processes are known. We estimated the lifetime egg production of the tellinid bivalve Macoma balthica at 11 sites over a tidal gradient in the western Wadden Sea, using a 30-year data series. The difference in individual lifetime egg production between the best sites in the lower tidal zone and the poorest sites on the high tidal flats was about a factor 10. The differences in lifetime egg production were related to differences in growth and, more importantly, survival. We argue that the large observed differences in reproductive output do not necessarily imply a lack of active habitat selection. As most animals start their last migration before final settlement from the high tidal flats, the choice may be one between a long and risky migration with a low chance of reaching the good habitat versus a more certain but poor existence on the high tidal flats.

Mosaic haploid-diploid embryos and polyspermy in the tellinid bivalve Macoma balthica.

We investigated meiosis, fertilization, and early development in eggs of the tellinid bivalve Macoma balthica (L.), which has external fertilization. Meiosis is standard but polyspermy is found to be very common. In all eight crosses examined, mosaic embryos consisting of a mixture of diploid (2n = 38) and haploid cells occur at a frequency ranging from 2.7 to 29.1%. The earliest mosaic found is in the two-cell stage. We propose that an androgenic haploid cell lineage can originate from one supernumerary sperm that decondenses into a functional haploid nucleus, starts mitosis, and is incorporated in the developing embryo.

Intertidal benthic resources of the Copper River Delta, Alaska, USA

The Copper River Delta, Alaska is the largest contiguous coastal wetland system along the West Coast of North America. Vast expanses of tidal mud flats formed by sediments carried by the suspended load of the Copper River serve as a connection between the Gulf of Alaska and the extensive network of wetlands, rivers and sloughs of the delta system. In addition to providing habitat for resident fish, shrimp and crabs, these tidal flats serve as critical feeding grounds for up to 5 million migratory shorebirds as well as an entry and exit corridor for three species of commercially fished salmonids. Here we report the first description of the benthic community of these intertidal flats. Between April and September 2000, we conducted three samplings on the Copper River Delta in which we quantified benthic macro-invertebrates inhabiting silt-clay sediments, the dominant substrate in the system, over a range of tidal inundation. Specifically, sampling was performed in two areas on the delta: near the outflows of the Eyak River and Pete Dahl Slough. Pore-water salinity of surficial sediment ranged from 4 psu during peak summer flow of the Copper River to 14 psu in April prior to increased riverine input. Sediment temperatures corresponded to ambient air temperatures with lowest temperatures during the April–September observation period recorded in April (4°C) and warmest in August (16°C). The benthic community of the delta's tidal flats was characterised by low species diversity and was dominated by the tellinid bivalve Macoma balthica, which reached densities greater than 4000 m −2. Age–length relationship of M. balthica indicated slow growth and longevity of up to 8 years. Polychaete densities, primarily the phyllodocid Eteone longa, were low throughout the study period, reaching a maximum of only 700 m −2 in August. Amphipod densities, primarily the corophid amphipod Corophium salmonis, were high (up to 7000 m −2) only during the August sampling. Spatial patterns of benthic invertebrate abundance were best explained by differences in tidal inundation with longer inundation corresponding to greater invertebrate densities. Temporal changes in abundance of polychaetes, amphipods, and M. balthica recruits corresponded to increases in sediment temperatures. Natural or human-induced changes to M. balthica populations could impact the food web of the delta, which could cascade to larger geographic impacts because of the importance of the delta to migratory species.

Maximizing lifetime egg production in a Wadden Sea population of the tellinid bivalve Macoma balthica: a trade-off between immediate and future reproductive outputs

The number of eggs produced in the annual spawning season by an adult female Macoma balthica (L.) of Wadden Sea origin increases in a non-linear manner with increasing shell length and body weight. It depends primarily on the weight-at-length immediately before spawning. Lean individuals with a low body-mass index (BMI) of 5.6 mg cm -3 or less spawn no eggs. Gamete output increases to about one-third of soft-body weight (in the order of 100 000 eggs) at the maximal BMIs observed (~15 mg cm -3 ). Long-term monitoring (>20 yr) of densities of a Wadden Sea M. balth- ica population revealed that survival to the spawning season of the next year declined from about 65% at higher-than-average values of BMI (>8 mg cm -3 ) to about 30% at the lowest values of BMI observed (5 to 6 mg cm -3 ). Annual growth was also significantly lower in years starting with a low BMI value. Because spawning lowers body weight and thus the BMI, spawning is bound to reduce subsequent survival rates and body-weight increments. Thus, a trade-off situation exists between immediate and future spawning outputs. The consequences for total lifetime egg production of vari- ous levels of gamete output at first spawning (at an age of 2 yr) were estimated by model calculations, starting from a wide range of body weights at a standard length. The model results realistically pre- dict that maximal lifetime egg production can be achieved only if M. balthica refrain from spawning at BMIs below a certain threshold value (viz. ~6 mg cm -3 , which is close to their actual threshold of 5.6 mg cm -3 ) and if their spawning output increases with weight-at-length (again in a manner close to what actually happens). It is concluded that M. balthica populations in the Wadden Sea apply a spawning strategy adapted to the local conditions.

The geographic scale of synchronized fluctuation patterns in zoobenthos populations as a key to underlying factors: climatic or man-induced

Densities of zoobenthic species observed at diVerent locations tend to fluctuate in parallel even when these sites are far apart. Climatic factors can synchronize population changes over wide geographic areas if they have a direct eVect on recruitment or mortality. Several examples indicate that severe winters represent a major synchronizing factor among many of the zoobenthos species of tidal flats, both by immediately enhanced mortality rates in species sensitive to low temperatures and by enhanced recruitment in bivalve species some months later. Long-term monitoring in three areas of the Wadden Sea (Balgzand, Groningen, and Norderney) revealed synchronous baseline patterns in the fluctuations of several species. Examples are shown for the polychaete Nephtys hombergii and the tellinid bivalve Macoma balthica. Local departures from such common patterns indicate local disturbing factors. Examples are shown on scales of about 1 km (a waste-water discharge) and several tens of kilometres (eutrophication in the westernmost part of the Wadden Sea). ? 1996 International Council for the Exploration of the Sea

Year-to-year variability in the biomass of macrobenthic animals on tidal flats of the Wadden Sea: How predictable is this food source for birds?

The Wadden Sea is important as a stop-over and wintering area for several species of waders, foraging for shorter or longer times on its tidal flats. The size of the food stocks these birds encounter varies from place to place and from year to year. We studied characteristics of the variability in time of such prey stocks, using long-term data series of annual estimates of biomass of macrobenthic animals collected on tidal flats in various parts of the Dutch and German Wadden Sea. Year-to-year fluctuations were stronger in nearly all individual benhos species than in total macrozoobenthic biomass. The various species differed significantly in their year-to-year variability. Everywhere the tellinid bivalve Macoma balthica was relatively stable, whereas species such as the cockle Cerastoderma edule and the polychaetes Lanice conchilega, Nephtys hombergii and Anaitides mucosa fluctuated heavily and rapidly in all parts of the Wadden Sea where they were found. Within species, fluctuations in biomass of individual age or size classes were stronger than those in total biomass of the species. Several species showed minimal biomass values in the same years over vast areas. This synchronization of scarcity was caused particularly by similar responses to winter character, which was each year similar over the entire Wadden Sea. Such similar responses included low over-winter survival during severe winters and recruitment failure after exceptionally mild winters. Immediately after severe winters, such cold-sensitivee species as C. edule, L. conchilega and N. hombegii were scarce all over the Waden Sea, thus liimiting the possibilities for birds to switch to other parts of the Wadden Sea to find their preferred prey in sufficient quantitu. Simultaneous recruitment failure in several important bivalve species ( C. edule, Mytilus edulis, and Mya arenaria limited the possibility for specialized bivalve consumers to switch to alternative prey types in certain years.

Effects of the deposit-feeding benthic bivalve Macoma balthica on meiobenthos.

To evaluate the effects of a deposit-feeding bivalve on meiobenthic assemblage structure in muddy habitats, a laboratory experiment was performed at the Askö Laboratory in the northwestern Baltic proper. Microcosms, surface area 104 cm2, containing a c. 7-cm thick layer of sieved (0.5 mm) sublittoral mud were established in June 1990. Two months later the tellinid bivalve Macoma balthica was added in quantities varying from 0 to 40 individuals per microcosm. After 5 months the effects of the bivalves on the meiofauna were surprisingly small. The density of harpacticoid copepods was lowest (P <0.05) in microcosms containing a high density of M. balthica. It is suggested that competition for food resources was responsible for this pattern. For all other meiofaunal groups, including nematodes which were the most abundant taxon (99%), no significant differences (P>0.05) were observed among treatments. The assemblage structure of the nematodes was similar between treatments. The vertical distribution of both major taxa and nematode species appeared to be unaffected by the presence of the bivalve.

Passive settlement of Macoma balthica spat on tidal flats of the Wadden Sea and subsequent migration of juveniles

Spatfall of the tellinid bivalve Macoma balthica may occur in fine-grained sediments at different tidal elevations in the Wadden Sea. but it is not clear which mechanism (active habitat selection or passive sinking of larvae, or both) can explain the observed distribution pattern. Spatfall and the subsequent development of juvenile abundances and size distribution were studied along a transect in the northern Wadden Sea near the Island of Sylt. Initial spatfall was highest in the lower intertidal and correlated significantly with hydrographic parameters. The enhanced larval settlement observed in dense aggregates of the tube-building polychaete Lanice conchilega confirmed the prominent role of hydrographic factors in initial spatfall. Subsequently, abundance strongly decreased in the lower intertidal but increased in the upper intertidal due to immigration of newly settled spat from lower sites. By the end of October, abundance was higher in the upper intertidal. Growth of the juveniles was higher in the upper intertidal. It is suggested that (1) initial spatfall is mainly ruled by hydrographic factors without active sediment selection; (2) young Macoma remain highly mobile during the first weeks of their benthic life and by byssus drift may achieve a net transport into areas with weak initial spatfall; (3) at the end of their first winter a second period of high floating activity occurs, bringing them back towards the lower intertidal and shallow subtidal. Thus, by successive postlarval migrations Macoma may several times change the intertidal site occupied during their first year of life. The comparatively low interannual variability of recruitment success noted in this species in the Wadden Sea may be a result of these migrations.

Genetic affinities of the bivalve Macoma balthica from the Pacific coast of North America: evidence for recent introduction and historical distribution

The tellinid bivalve Macoma balthica (L.) has an extensive geographic range that reaches from temperate to arctic coastal waters in the North Atlantic and North Pacific oceans. Recent studies have indicated that eastern and western North Atlantic populations are morphologically and genetically different from one another, and that they may have diverged as sibling species. To determine the genetic relationship between M. balthica from the Pacific and Atlantic coasts of North America, populations from each coast were examined at 11 enzyme loci using standard starch gel electrophoresis. Allele frequency data indicate that M. balthica populations from San Francisco Bay, California appear more closely related to western North Atlantic populations than to populations from Oregon. We suggest that San Francisco Bay populations were introduced relatively recently from western North Atlantic populations. The Oregon populations are probably a natural extension of northern populations that occur along Northern Asia and in the eastern North Atlantic.

Floating behaviour in the tellinid bivalve Macoma balthica (L.).

The tellinid bivalve Macoma balthica from the Dutch Wadden Sea mudflats achieved secondary distribution by a floating behaviour after stimulation by low ambient temperature in slow-moving sea water (salinity 25‰). Floating behaviour among responding mussels began with burrowing displacements as their foot was directed towards the sediment surface. After extreme protrusion of the foot they became buoyant and were able to float. Floating behaviour was observed to last for periods of 1.5 h. During this active sequence frequent stops (range 2-6) were followed by resting periods on the sediment. In stagnant water at a constant temperature, mussels displayed burrowing displacement in a rhythmic manner with one peak of activity during the dark period of the day. Mussels previously acclimatized at high temperatue showed significantly stronger responses to current and temperature stimuli. Adult mussels as well as juveniles performed the floating behaviour. The paper discusses the ecological significane of secondary distribution.

Single and dual annual growing seasons in the tellinid bivalve Macoma balthica (L.)

Seasonal patterns of changes in length and weight during their second year of life were studied in two intertidal populations of the tellinid bivalve Macoma balthica (L.), viz. in The Netherlands (Wadden Sea) and in France (Seine estuary). The Wadden Sea population showed a single and short annual period of growth in spring (March through June), followed by a long annual period of nearly stagnant length growth and loss of weight of the soft parts. The Seine population started to grow earlier in the year (February), likewise retarded growth in summer, but restarted in autumn, thus showing a dual annual growing season with periods of rapid gain of length and weight both during spring and in October. The timing and the presence and absence of a second annual growing season are discussed in relation to temperature and feeding conditions in the various habitats.

Effects of temperature on the length of the annual growing season in the tellinid bivalve Macomabalthica (L.) living on tidal flats in the Dutch Wadden Sea

Frequent inspection of the shell margins during a 15-yr study of tidal flat populations of Macoma balthica (L.) in the western part of the Wadden Sea revealed that the annual growing season starts earlier (viz. early March compared with late March) if preceding winter temperatures were higher. The reversal of weight gain to weight loss used as an indicator of the end of the growing season occurs earlier in July if early-summer temperatures are higher. Thus, growth is restricted to the range of water temperatures between 4 and 16°C in spring. No growth was observed during the autumn at the same temperatures. Although low and high temperatures appear to delimit the annual spring growing season, total annual growth is not related to the length of the growing season nor to temperatures prevailing during this period. Feeding conditions appear to prevent growth in autumn and determine the highly variable growth rates within the temperature-set growing period in spring.

Growth and recruitment of the tellinid bivalve Macoma balthica at the southern limit of its geographical distribution, the Gironde estuary (SW France)

Growth of the bivalve Macoma balthica (L.) has been studied in 3 intertidal populations in the Gironde estuary, South-West France. This locality is supposed to be at the southern limit of the zoogeographical range of this species in the European waters. Investigations on the annual reproductive cycle and the seasonal evolution of a condition factor indicate a protracted spawning period from the spring to the autumn, giving 2 or 3 settlements per year. The main growth in length occurs between April and July–August. Growth is faster during the first growing season, the recently settled individuals being 3 to 8 mm in length during the first winter after settlement; growth then regularly decreases with increasing age. Growth rates are not affected by salinity but are significantly higher in high intertidal areas than at the low-water level. Theoretical growth equations (von Bertalanffy, Gompertz and logistic curves) were used to describe growth in M. balthica. The von Bertalanffy model gives an adequate description of growth during the life span of an individual, but a better fit is found with incorporation of temperature in the von Bertalanffy equation. Using published data on rates of growth of M. balthica, the growth constant K of von Bertalanffy was computed for populations located on a wide geographical range. A linear relationship was found between K and the latitude, suggesting a dependence of growth on latitude and temperature.

Calorific values of the soft parts of the tellinid bivalve Macoma balthica (L.) as determined by two methods

Calorific values of the ash-free dried soft parts of Macoma balthica (L.), sampled monthly during 1 year at a tidal flat station in the Dutch Wadden Sea, have been estimated by two methods. The indirect method started from an analysis of the biochemical composition and used conversion factors for the various components to calculate the calorific value of the total tissue. The direct method employed a micro-bomb calorimeter and a furnace for separate ash determinations. The indirect method yielded estimates that were consistently higher than those from the direct one. Two sources, explaining most of the difference, could be traced, viz. incomplete drying of the samples used in the calorimeter and a too high conversion factor for weight to calories applied conventionally for lipids. This conversion factor was found to depend on the method of extraction of the lipids. but was always significantly below the commonly used 9.3 to 9.7 cal · mg −1. The best estimates for the annual mean of the calorific value at complete combustion of the ash-free and well-dried soft parts of Macoma were 5.47 for the direct and 5.59 cal·mg −1 ash-free dry wt for the indirect method. Both values are higher than estimates for Macoma published earlier by various authors. Calorific values at physiological oxidation amount to only about 4.6 cal·mg −1 or less, due to incomplete protein oxidation. For this reason, it is concluded that biologically significant calorimetry cannot dispense with biochemical analysis. On the other hand, calculation of calorific values from biochemical composition should be accompanied by some calorimetry, as the conversion factor for the lipid fraction, at least, may deviate significantly from commonly applied values.