Introduced Pacific oysters (Crassostrea gigas) in the northern Wadden Sea: invasion accelerated by warm summers?

Among the increasing number of species introduced to coastal regions by man, only a few are able to establish themselves and spread in their new environments. We will show that the Pacific oyster (Crassostrea gigas) took 17 years before a large population of several million oysters became established on natural mussel beds in the vicinity of an oyster farm near the island of Sylt (northern Wadden Sea, eastern North Sea). The first oyster, which had dispersed as a larva and settled on a mussel bed, was discovered 5 years after oyster farming had commenced. Data on abundance and size-frequency distribution of oysters on intertidal mussel beds around the island indicate that recruitment was patchy and occurred only in 6 out of 18 years. Significant proportions of these cohorts survived for at least 5 years. The population slowly expanded its range from intertidal to subtidal locations as well as from Sylt north- and southwards along the coastline. Abundances of more than 300 oysters m^–2 on mussel beds were observed in 2003, only after two consecutive spatfalls in 2001 and 2002. Analyses of mean monthly water temperatures indicate that recruitment coincided with above-average temperatures in July and August when spawning and planktonic dispersal occurs. We conclude that the further invasion of C. gigas in the northern Wadden Sea will depend on high late-summer water temperatures.Communicated by H.D. Franke     

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

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

Introductions and developments of oysters in the North Sea area: a review

To replenish the exploited native stocks ofOstrea edulis, imports from almost all European coasts have arrived in the North Sea, particularly in the Dutch Oosterschelde estuary. The American oysterCrassostrea virginica and the Portuguese oysterC. angulata have also been imported into the North Sea several times. However, only the introductions of various genetic strains of the Pacific oysterC. gigas have been of lasting success. Spat from British Columbia (Canada) was first imported to the Oosterschelde in 1964. First spatfalls in this area took place in the warm summers of 1975 and 1976. Further larval outbursts occurred in 1982 and 1989, and good settlements took place on culture plots as well as along the dikes of the Oosterschelde. Since 1977 no more cupped oysters have been imported from overseas. The population maintained itself and was able to spread in a northern direction along the Dutch North Sea coast. In Britain, hatchery-producedC. gigas were transferred to several sites, in the 1970s including the British North Sea coast. Here, occurrence in the wild seems to be rather limited up to now. Into the German Wadden Sea,C. gigas larvae and spat from a Scottish hatchery have been introduced since 1971, as were medium-sized oysters from a variety of European sources in the 1980s. Strong spatfalls on intertidal mussel beds in the northern German Wadden Sea occured in 1991 and 1994. For the introductions ofC. gigas along the west European coasts, precautionary measures to minimize unintentional transfers of associated organisms, as recommended by the ICES Code of Practice in 1994, came too late.     

Changes in the waterbird populations of the Oosterschelde (SW Netherlands) as a result of large-scale coastal engineering works

Between 1982 and 1987, the construction of a storm-surge barrier and two secondary dams in the eastern and northern parts of the Oosterschelde/Krammer-Volkerak area resulted in the loss of 33% of the 170 km² of intertidal area in the estuary. Consequences for non-breeding waterbirds were evaluated on the basis of monthly high-tide counts during five seasons before and three seasons after the construction period.In the entire Oosterschelde/Krammer-Volkerak area, numbers of wintering waders decreased but those of ducks increased. Peak numbers and total number of bird-days changed little, but the seasonal pattern shifted from a midwinter maximum to a peak in autumn.In the Oosterschelde (excluding the Krammer-Volkerak), where 17% of the tidal flats disappeared, species feeding mainly on open water remained stable or increased. Species dependent on intertidal areas for foraging (mainly waders and dabbling ducks) generally decreased. Total density of intertidal foragers decreased slightly. In most intertidal species, the Oosterschelde wintering population showed a stronger decrease, or smaller increase, than was shown during the same period by numbers in Britain and Ireland which were taken as an index of the total W-European winter populations. Changes varied considerably between species, and were correlated with their distribution within the estuary. Species concentrated in the eastern sector, where most habitat loss occurred, declined more than species with a more westerly distribution.Results indicate that intertidal foragers forced to move from the enclosed parts of the estuary were not generally able to settle into the remaining intertidal areas. Both dispersal to adjacent areas (mainly by dabbling ducks) and mortality during severe winter weather (in some wader species) may have contributed to the declines. Populations of intertidal foragers apparently were (and consequently still are) close to carrying capacity, and further changes in capacity, as foreseen from geomorphological changes still under way in the estuary, are likely to be reflected in bird populations.Numbers of waders moulting in the Oosterschelde in late summer declined strongly compared to numbers in other seasons. Increased disturbance due to recreational activities may have played a role during this time of the year.     

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

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

High survival and growth rates of introduced Pacific oysters may cause restrictions on habitat use by native mussels in the Wadden Sea

Pacific oysters Crassostrea gigas (Thunberg, 1793) were introduced to the northern Wadden Sea (North Sea, Germany) by aquaculture in 1986 and finally became established. Even though at first recruitment success was rare, three consecutive warm summers led to a massive increase in oyster abundances and to the overgrowth of native mussel beds (Mytilus edulis L.). These mussels constitute biogenic reefs on the sand and mud flats in this area. Survival and growth of the invading C. gigas were investigated and compared with the native mussels in order to predict the further development of the oyster population and the scope for coexistence of both species. Field experiments revealed high survival of juvenile C. gigas (approximately 70%) during the first three months after settlement. Survival during the first winter varied between > 90% during a mild and 25% during a cold winter and was independent of substrate (i.e., mussels or oysters) and tide level. Within their first year C. gigas reached a mean length of 35-53 mm, and within two years they grew to 68-82 mm, which is about twice the size native mussels would attain during that time. Growth of juvenile oysters was not affected by substrate (i.e., sand, mussels, and other oysters), barnacle epibionts and tide level, but was facilitated by fucoid algae. By contrast, growth of juvenile mussels was significantly higher on sand flats than on mussel or oyster beds and higher in the subtidal compared to intertidal locations. Cover with fucoid algae increased mussel growth but decreased their condition expressed as dry flesh weight versus shell weight. High survival and growth rates may compensate for years with low recruitment, and may therefore allow a fast population increase. This may lead to restrictions on habitat use by native mussels in the Wadden Sea.     

Physical constraints on the foraging ecology of a predatory snail

We studied the effects of aerial exposure and high summer temperatures on the southern oyster drill ( Stramonita haemastoma ), feeding on the American oyster, Crassostrea virginica . In the laboratory, oyster drill feeding rates and growth were highest at 25 and 30°C, some mortality occurred at 35°C, all snails died at 40 and 45°C, and the 28-day LC 50 was 35.7°C. In a second experiment where both water temperature (25 vs . 33°C) and aerial exposure were varied, only simulated tidal exposure lowered oyster drill feeding and growth rates. In field cage experiments, oyster drills had reduced feeding rates and growth at intertidal sites, but snail growth rates increased in late summer with warmer water temperature. We therefore conclude that aerial exposure, not high temperature, is the major factor limiting oyster drill feeding and growth in intertidal oyster reefs. Field experiments with partial cages also suggested that ambient predation rates were much higher at a subtidal than at a nearby intertidal site. Because southern oyster drills have depressed feeding, growth, and possibly lower fitness in intertidal oyster reefs during the summer, this reduced predation risk may provide a refuge for intertidal oysters.     

Exploring the decline of oyster beds in Atlantic Canada shorelines: potential effects of crab predation on American oysters (<Emphasis Type="Italic">Crassostrea virginica</Emphasis>)

Atlantic Canada’s American oyster (Crassostrea virginica) beds, while economically and ecologically important, have been in decline over the past few decades. Predation by crabs, in particular by the European green crab (Carcinus maenas), has been proposed as one of the potential causes of such decline. Hence, this study examined oyster mortality levels in multiple beds across Prince Edward Island (PEI) and then experimentally assessed the contribution of green crab predation to oyster mortality. Results from surveys conducted in 10 estuaries across PEI in 2014 indicate that the probability of mortality for small oysters was significantly higher when green crabs were present then in areas without green crabs. This probability of mortality was significantly less when there was the presence of alternative prey like natural mussel beds (Mytilus edulis). The odds of oyster mortality were also higher when beds had rock crabs (Cancer irroratus) compared to beds with no rock crabs. Given the potential importance of green crab predation, its influence was assessed in 2015 using two field experiments with tethered oysters. Our results indicate that odds of small oyster mortality occurring were much higher in green crab inclusion cages than in the open environment and the exclusion cages. These results reaffirm that oysters up to ~40 mm SL are vulnerable to predation, and at least some of the mortality affecting these oysters can be causally attributed to green crab predation. Green crab predation rates upon small oysters are relevant given the economic benefits and ecosystem services provided by these bivalves. They highlight the need for the industry to consider mitigation measures and potentially adapt their oyster growing strategies.     

Variations in the intertidal and subtidal macrofauna and sediments along a salinity gradient in the upper forth estuary

The intertidal and subtidal soft-sediment macrofauna of the upper Forth estuary, eastern Scotland, UK has been examined. The intertidal fauna was sampled in 1977, and again in 1988/89, at up to twelve stations along the salinity gradient. The subtidal fauna was sampled in 1982 and in 1988/89 at up to 15 stations. The stations span the region of the freshwater-seawater interface, and area of the turbidity maximum. Large spatial and temporal variations in macrofaunal abundance and species composition were observed. Sites at the head of the estuary with low salinity were dominated by oligochaetes, but more saline areas were characterised by a depauparate estuarine fauna. The area has historically received large quantities of organic waste both from sewage and industrial discharges which supported very high abundances of oligochaetes of up to 500,000 m⁻² in the upper reaches of the estuary. Reductions in the organic inflow to the area since the early-1980's have begun to cause reductions in oligochaete populations and also allowed the further penetration intertidally of non-oligochaete species into the upper and middle reaches of the estuary. No comparable upstream penetration by the non-oligochaete subtidal fauna has been observed, possibly on account of the greater sediment instability in the estuary's main channel.     

The European oyster <Emphasis Type="Italic">(Ostrea edulis)</Emphasis> and its epibiotic succession

This study aimed to investigate intra- and inter-site differences in the epibiota on the European oyster Ostrea edulis of different ages and on hard substrata to assess their contribution to biodiversity. This research has shown that shells of O. edulis do show higher species diversity than non-living hard substrata and as oysters grow larger epibiotic diversity will increase. This investigation has revealed that O. edulis possesses biogenic engineering qualities and the value of O. edulis as a vehicle for increasing biodiversity should not be underestimated. Relatively few studies have examined the shell surfaces of Ostrea edulis, which, together with their associated epifauna provide a large portion of the natural hard substrata for sessile filter-feeding organisms, including oysters, in coastal and estuarine ecosystems. It can be considered a keystone species which has an influence on intertidal and subtidal community structures.     

Habitat linkages: the effect of intertidal saltmarshes and adjacent subtidal habitats on abundance, movement, and growth of an estuarine fish

In this study we used pinfish (Lagodon rhomboides) in field experiments to examine linkages between intertidal saltmarsh and adjacent subtidal habitats. Pinfish are more than twice as abundant in intertidal marshes adjacent to seagrass beds than in those adjacent to the unvegetated subtidal bottom. Movement of pinfish between the marsh edge and the adjacent subtidal habitat was greater for fish captured in areas with both intertidal and subtidal vegetation than in those with intertidal vegetation and adjacent unvegetated mudflats. This movement provides an important link between habitats, allowing transfer of marsh-derived secondary production to subtidal seagrass beds and vice versa. Pinfish held in enclosures with both intertidal and subtidal vegetation were, on average, approximately 90% heavier than fish held in enclosures with intertidal vegetation and unvegetated subtidal bottom. Because saltmarshes and seagrass beds contribute to the production of living marine resources, active measures are being taken to preserve and restore these habitats. The results from this study have direct application to decisions concerning site selection and optimal spatial proximity of saltmarsh and seagrass habitats in the planning of restoration and mitigation projects. To maximize secondary production and utilization of intertidal marshes, managers may opt to restore and/or preserve marshes adjacent to subtidal seagrass beds. Received: 31 May 1996 / Accepted: 23 October 1996     

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

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

Biomonitoring of trace metal contamination in mangrove-lined Brazilian coastal systems using the oyster Crassostrea rhizophorae: comparative study of regions affected by oil, salt pond and shrimp farming activities

The oyster Crassostrea rhizophorae has been used as a biomonitor of trace metal contamination in two Brazilian coastal systems. C. rhizophorae were collected in January 1998 from 15 stations (from 4 coastal inlets (including 1 estuary) and 1 coastal beach) near Macau, Rio Grande do Norte (RN), Brazil, a region affected by the activities of the oil industry and salt manufacture in coastal salt ponds; oysters were also collected in September 1999 from 8 stations in the Curimatau estuary (RN), an estuary becoming increasingly affected by shrimp farming activities. C. rhizophorae is a net accumulator of trace metals and can be used as a biomonitor, the accumulated soft tissue concentrations representing integrated records of bioavailable metal over the life of the oyster. At Macau, significant differences in oyster accumulated concentrations (and hence bioavailabilities to the oyster) of Fe, Zn, Cu, and Mn were found between stations; raised zinc availabilities at the coastal site are in close proximity to oil industry activities but the very high availabilities of Fe, Cu and Mn in the Rio dos Cavalos estuary originate from an unknown source. In the Curimatau estuary, bioavailabilities of Mn, Pb and Cd, but particularly of Cu and Zn, to the oysters are raised at the two most downstream sites, the only sites below the effluent of a large shrimp farming enterprise. The oysters also act as a local food source, and concentrations of Zn, Cu and Pb of some of the oysters are above typical public health recommended limits.     

Oyster reef enhancement utilizing gardened oysters in a subtropical estuary

Crassostrea virginica, the eastern oyster, is a native foundational species that inhabits coastal and estuarine ecosystems along the western Atlantic seaboard. Introduction of C. virginica into estuarine areas with limited or no extant populations is gaining popularity as a pro‐active approach for improving estuarine water quality and creating natural wave breaks for shoreline stabilization. Adult oysters, grown by 113 community members under their private docks, were collected and deployed at three county‐owned sites along the Indian River Lagoon within Brevard County, Florida. In this shallow, warm‐water estuary, replicate treatments deployed at each site included bagged adult oysters collected from gardeners in fall 2014, bagged adult oysters from spring 2015 gardeners, bagged blank (clean) shell, and empty plots (control). Prior to deployment, morphometric data (shell length, weight) were collected on all gardened oysters. Morphometric data were then collected quarterly for all surviving and recruited oysters for 18 months. Our monitoring timeframe was sufficient for assessing survival of gardened oysters, but likely not sufficient to understand recruitment patterns. In areas with no recruitment and limited gardened oyster survival, regular enhancement with live oysters would be needed for long‐term success. In areas with natural recruitment, the blank shell treatment was most successful. Lessons learned from this study include: (1) need for better tracking of abiotic variables (e.g. salinity) where gardening occurred, (2) role of seasonality in initial post‐deployment survival, even in a warm‐water estuary, and (3) importance of pilot studies prior to large‐scale gardened oyster deployments.     

Intertidal community structure differs significantly between substrates dominated by native eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.) and adjacent to the introduced oyster <Emphasis Type="Italic">Crassostrea gigas</Emphasis> (Thunberg) in British Columbia,Canada

Eelgrass beds represent important habitats for marine organisms, but are in decline in many coastal areas around the world. On Cortes Island, British Columbia, Canada, oysters coexist regionally with native eelgrass (Zostera marina L.), but eelgrass is typically absent directly seaward of oyster beds (the “below-oyster cobble zone”). We compared assemblage structure of nekton (fish and swimming macroinvertebrates) and epibenthos (macroinvertebrates and macroalgae) between eelgrass bed and below-oyster habitats. We sampled the intertidal zone on Cortes Island at low tide using two methods: quadrats to enumerate epibenthic macroinvertebrates and macroalgae, and beach seines to enumerate fish and swimming macroinvertebrates. Using multivariate analysis of similarity (ANOSIM), we found that the structure of nektonic and epibenthic assemblages associated with below-oyster cobble zones were significantly different from those in eelgrass-beds. Univariate measures showed that nektonic species richness and abundance were significantly higher in eelgrass beds than in below-oyster cobble habitat, whereas epibenthic species richness and abundance were significantly higher in below-oyster habitat. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: J. Trexler     

Direct effects of physical stress can be counteracted by indirect benefits: oyster growth on a tidal elevation gradient

The paradigmatic gradient for intertidal marine organisms of increasing physical stress from low to high elevation has long served as the basis for using direct effects of duration of water coverage to predict many biological patterns. Accordingly, changes in potential feeding time may predict the direction and magnitude of differences between elevations in individual growth rates of sessile marine invertebrates. Oysters (triploid Crassostrea ariakensis) experimentally introduced at intertidal (MLW+0.05 m) and subtidal (MLW–0.25 m) elevations in racks provided a test of the ability to use duration of water coverage to predict changes in growth. During early-to-mid winter, a depression of 38–47% in shell growth of intertidal oysters matched the 36% reduction in available feeding time relative to subtidal oysters. In late winter as solar heating of exposed oysters increased, growth differences of 52–55% departed only slightly from the predicted 39%. In spring, however, duration of water coverage failed to predict even the correct direction of growth change with elevation as intertidal oysters grew 34% faster despite 39% less feeding time. Intense seasonal development of shell fouling by other suspension feeders like ascidians, mussels, and barnacles on subtidal (94% incidence) but not on aerially exposed intertidal (21–38% incidence) oysters may explain why duration of water cover failed to predict spring growth differences. Less intense fouling develops on intertidal oysters due to the physiological stress of aerial exposure on settlers, especially during higher temperatures and longer solar exposures of spring. Fouling by suspension feeders is known to reduce growth of the host through localized competition for food and added energetic costs. Thus, in springtime, indirect effects of aerial exposure providing a partial refuge from biological enemies overwhelmed direct effects of reduced duration of water coverage to reverse the expected pattern of slower intertidal growth of a marine invertebrate.     

A preliminary study on the effects of oyster culturing structures on birds in a sheltered Irish estuary

This study investigated the species composition, numbers and behaviour of birds in an intertidal oyster culture area in Cork Harbour . These data were compared to a nearby area free of aquaculture within the same estuary in March 1999. Species which occurred in the aquaculture free area were also observed in the trestle-area. The most abundant species were oystercatcher Haematopus ostralegus, redshank Tringa totanus, dunlin Calidris alpina, curlew Numenius arquata, black-headed gull Larus ridibundus and common gull Larus canus. Oystercatcher, curlew, black-headed gull and common gull occurred in significantly lower numbers in the trestle area, while for redshank and dunlin the differences were not significant. The percentage of birds feeding did not differ between the two areas. Oystercatcher, redshank, dunlin and curlew mostly fed in both areas. In contrast, black-headed gull and common gull generally did not feed, but surveyed the area. Whether the trestles were covered by oyster bags or not did not have any effect on the number of birds except for the dunlin. Dunlin were significantly more frequent beneath the trestles with bags compared with those without bags. In general, the percentage of birds feeding did not differ between areas. Interspecies differences occurred with regard to the position occupied by birds at the trestles. Oystercatcher, redshank and curlew spent more time underneath the trestles. Dunlin, black-headed gulls and common gulls did not differ in numbers underneath or on top of the trestles. These preliminary observations at a single time period give some insight as to the potential interactions between shellfish aquaculture and intertidal birds.     

Tidal reduction and its effects on intertidal hard-substrate communities in the Oosterschelde estuary

Developments of intertidal hard-substrate communities in the Oosterschelde estuary were examined in perpendicular transects between high-water line and low-water line in the period 1982–1992. Prior to the beginning of the Oosterschelde estuary works a typology of communities was established and an overall survey of the estuary was carried out. The communities contain flora (algae) as well as fauna. Due to asphalting of dikes in 1986, much of the surface of several communities has been destroyed. The originally well developed communities with large species-richness have not returned. The small reduction in tidal amplitude due to the construction of the storm-surge barrier had a minor effect on the zonation of communities. In the upper part of the intertidal zone the boundaries of the communities moved 0.5–1.0 m downward in the transects along the dike-slopes. At an average inclination of 18° this means a vertical shift of about 15–30 cm. This reflects the reduction of the tidal amplitude: the high-water line shifted ca 22 cm downward. In a number of places sedimentation has caused a reduction in the number of smaller seaweed species in the lower eulittoral zone. At monitoring locations presence of the original communities is rather unchanged. Rare species like Pelvetia canaliculata, Actinia equina and Gelidium pusillum have been able to maintain quite successfully.